Comparative structure and evolution of the organellar genomes of Padina usoehtunii (Dictyotales) with the brown algal crown radiation clade

Comparative structure and evolution of the organellar genomes of Padina usoehtunii (Dictyotales) with the brown algal crown radiation clade | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Comparative structure and evolution of the organellar genomes of Padina usoehtunii (Dictyotales) with the brown algal crown radiation clade Yi-Jia Liu, Tong-Yun Zhang, Qi-Qi Wang, Stefano G.A. Draisma, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3835960/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 31 Jul, 2024 Read the published version in BMC Genomics → Version 1 posted 8 You are reading this latest preprint version Abstract Background Organellar genomes have become increasingly essential for studying genetic diversity, phylogenetics, and evolutionary histories of seaweeds. The order Dictyotales (Dictyotophycidae), an early-diverging and highly diverse lineage within the Phaeophyceae, is long-term characterized by a scarcity of organellar genome datasets compared to orders of the brown algal crown radiation (Fucophycidae). Results We sequenced the organellar genomes of Padina usoehtunii , a representative of the order Dictyotales, to investigate the structural and evolutionary differences by comparing to five other major brown algal orders. Our results confirmed that the rate of structural rearrangements in chloroplast genomes is higher than that in mitochondria, whereas mitochondrial sequences exhibited a higher substitution rate compared to chloroplasts. Such evolutionary patterns contrast with land plants and green algae. The expansion and contraction of the inverted repeat (IR) region in the chloroplast correlated with the changes in the number of boundary genes. Specifically, the size of the IR region influenced the position of the boundary gene rpl 21, with complete rpl 21 genes found within the IR region in Ectocarpales, while the rpl 21 genes in Desmarestiales, Fucales, and Laminariales span both the IR and short single copy (SSC) regions. The absence of the Rbc R and rpl 32 genes in the Dictyotales may indicate a horizontal transfer from the chloroplast to the nuclear genome. Inversion of the SSC region occurred at least twice in brown algae. Once in a lineage only represented by the Ectocarpales in the present study and once in a lineage only represented by the Fucales. Photosystem genes in the chloroplasts experienced the strongest purifying selection, while ribosomal protein genes in both chloroplasts and mitochondria underwent a weak purifying selection. Conclusions Variations in chloroplast genome structure among different brown algal orders are evolutionarily linked to their phylogenetic positions in the Phaeophyceae tree. Structural variability to some extent is an inherent mechanism to create genetic diversity of brown algal taxa. Different functional gene categories in organelles exhibit varying degrees of structural variation and distinct patterns of sequence evolution, potentially giving rise to new genes adapted to various environmental pressures. Padina usoehtunii Dictyotales Phaeophyceae chloroplast genome mitochondrial genome phylogeny structural variation sequence variation Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Background Semi-autonomous organelles in plant cells arose from ancient endosymbiotic events and subsequently underwent multiple gene transfers and structural modifications [ 1 , 2 , 3 ]. Through this evolutionary process, organellar genomes have retained genes for essential organellar functions. Nowadays, with the increased availability of organellar genomes, it has become technically feasible to investigate genome-scale evolution, adaptation, and phylogenetic diversity across the algae tree of life. The brown algae or Phaeophyceae form a class of multicellular heterokont algae, currently classified into twenty orders and over 2,000 species [ 4 ]. They often represent an essential component of the littoral and sublittoral zones in temperate and tropical ecosystems. This ancient and diverse lineage originated approximately 185 − 180 million years ago (Ma) [ 5 ]. In brown algae, fossil evidence, including Padina (Dictyotales; 145.5–99.6 Ma) [ 6 ], Paleocystophora (Fucales) and Julescraneia grandicornis (Laminariales; 13–17 Ma) [ 7 ], along with the estimates of concatenated organellar genes [ 8 , 9 ], suggest that the orders Dictyotales and Sphacelariales evolved earlier (> 100 Ma) than Desmarestiales/Laminariales/Ectocarpales (< 100 Ma) [ 10 ]. The estimated brown algal divergence times reported that the order Dictyotales is a member of the SSDO clade (Sphacelariales, Syringodermatales, Dictyotales, and Onslowiales) or Dictyotophycidae that split from the BACR clade (brown algal crown radiation) or Fucophycidae and diversified into orders during the Jurassic (200 − 175 Ma) [ 5 ]. Ectocarpales, Laminariales s.l. , Fucales, and Desmarestiales belonging to the BACR clade, diversified into orders during the early Cretaceous period (128 Ma). Taxonomically, the identification and classification of new brown algal species primarily relies on morphological characteristics and DNA sequences. Organellar genes in particular have shown better resolution for intraspecific discrimination in certain taxonomic groups compared to the nuclear internal transcribed spacer (ITS) [ 11 ]. They have provided essential insights into the origin, phylogenetic structure and biogeographical patterns of brown algae [ 5 , 11 , 12 , 13 , 14 , 15 , 16 ]. The application of organellar genomes has also been proved instrumental to uncover genetic relationships among individuals and populations, shedding light on adaptive evolution [ 17 ]. Most phaeophycean organellar genomes sequenced to date are from members of the Fucophycidae (BACR clade) and only three species of Dictyotophycidae (SSDO clade), one Ishigeophycidae and no Discosporangiophycidae [ 18 ]. Notably, the structural and functional interpretation and comparison of the available organellar genomes seldom connected to the phylogenetic structure and timing of the brown algal tree of life. For example, a comparative study of mitochondrial and chloroplast genomes of Sargassum confusum (Fucales) found distinct evolutionary characteristics between the two organellar genomes in terms of A + T content, intron content, and stop codon usage, and reported that mitochondrial genomes exhibited more nucleotide variability than the chloroplast[ 19 ]. In addition, the estimated base substitution rates among seven Sargassum species in the Phaeophyceae showed higher mutation rates of mitochondrial genes compared to chloroplast genes [ 20 ]. A more recent study of organellar genome rearrangements and evolution in nine orders of brown algae found that mitochondrial genes evolved at a faster rate than chloroplast genes, but that structural rearrangements in chloroplast genomes were more prevalent than in mitochondria [ 18 ]. However, these studies either focused on a single genus or individual organellar genome, or biased taxa with data-rich organellar genomes. The limited number of organellar genomes from representatives outside the Fucophycidae may also lead to an incomplete or biased evolutionary interpretation of organellar genomes in the Phaeophyceae. To comprehensively elucidate the evolution and origin of brown algae, it is imperative to augment the organellar genome database from diverse brown algal taxa. The order Dictyotales represents a diverse and evolutionarily important lineage in the Phaeophyceae [ 21 ]. Dictyotalean species are widely distributed in subtropical and tropical oceans and constitute one of the few brown algal taxa with high diversity in the tropics due to the tolerance to a warm climate [ 22 ]. Among its diverse genera, the noteworthy genus Padina Adanson encompasses 58 currently accepted and formally described species [ 23 ], but 63 operational taxonomic units (OTUs) [ 21 ]. Padina usoehtunii Ni-Ni-Win & H.Kawai is only known from the west coast of the Southeast Asian peninsula, from the Bay of Bengal (Myanmar) to the Malacca Strait (Thailand) where it grows in the intertidal [ 24 , 25 , 26 ]. This species can potentially serve as a model for studying lineage diversity and genome evolution of brown algae. In this study, we sequenced the mitochondrial and chloroplast genomes of P. usoehtunii , thereby adding to the organellar genome dataset of the order Dictyotales, which had previously consisted of two species ( Dictyopteris divaricata (Okamura) Okamura and Dictyota dichotoma (Kuentze) O.Schmidt) within the family Dictyotaceae. Our study focused on the Dictyotales and compared it with five representative brown algal orders, i.e., Sphacelariales (Dictyotophycidae) and Desmarestiales, Laminariales s.l. , Ectocarpales, and Fucales (Fucophycidae). Mitochondrial genomes are available for two other orders (Ralfsiales, Ishigeales), but chloroplast genome are not available for these orders and therefore excluded from this study. Our investigation is centered on the following key aspects among brown algal organelles: 1) organellar genome features; 2) extent of structural rearrangements (inverted repeat regions and gene arrangements); 3) sequence evolutionary differences (nucleotide substitution rates, codon usage bias, and repeat sequences). Results Organellar genomes characteristics of Padina usoehtunii The single-circular chloroplast genome of P. usoehtunii is 125,291 bp in length (Fig. S1 ), larger than species of Fucales (124,068–125,066 bp), but smaller than any other previously sequenced brown alga (126,099–139,954 bp) (Table 1 ). The largest phaeophycean chloroplast genome (139,954 bp) is found in Ectocarpus siliculosus (Dillwyn) Lyngbye (Ectocarpales). The chloroplast genome of P. usoehtunii comprises a 72,226 bp Long Single Copy region (LSC), a 41,273 bp Short Single Copy region (SSC), and two 5,896 bp inverted repeats regions (IRa and IRb) (Fig. S1 ). It contains 173 genes accounting for 78.02% of the chloroplast genome, including 139 protein coding genes (PCGs), 28 transfer RNA (tRNA) genes, and 6 ribosomal RNA (rRNA) genes (Table S1 ). The rbc R and rpl 32 genes were lost in both dictyotaleans, P. usoehtunii and Dictyopteris divaricata , but present in all six other investigated orders. The thiS gene was absent in the Dictyotales, Desmarestiales, and Ectocarpales, and three species of Laminariales s.l. (i.e., Chorda asiatica , Laminaria ephemera , and Saccharina japonica ), but present in Fucales, Sphacelariales, and two species of Laminariales (i.e., Alaria marginata and Macrocystis pyrifera ). Table 1 General features of organelle genomes in Phaeophyceae. Species Order Family GenBank Mitochondrion GenBank Chloroplast CDs tRNAs rRNAs ORF Size(bp) CDs tRNAs rRNAs ORF Size(bp) Padina usoehtunii Dictyotales Dictyotaceae MW485979 36 25 3 1 32,303 MW485982 139 28 6 2 125,291 Dictyopteris divaricata Dictyotales Dictyotaceae NC_043845 38 24 3 3 32,021 NC_036804 139 27 6 2 126,099 Dictyota dichotoma Dictyotales Dictyotaceae NC_007685 38 24 3 3 31,617 Protohalopteris sp. Sphacelariales Stypocaulaceae MZ156064 a) 39 23 n.d. a) 6 41,306 MZ156028 144 28 6 2 131,355 Desmarestia aculeata Desmarestiales Desmarestiaceae MZ156052 39 25 3 3 40,822 MZ156041 142 28 6 1 129,228 Desmarestia viridis Desmarestiales Desmarestiaceae NC_007684 39 25 3 4 39,049 Sargassum serratifolium Fucales Sargassaceae NC_066463 37 25 3 2 34,793 NC_066459 139 28 6 2 124,514 Sargassum macrocarpum Fucales Sargassaceae NC_066462 37 25 3 2 34,766 NC_066458 139 28 6 2 124,517 Sargassum fulvellum Fucales Sargassaceae NC_066461 37 25 3 2 34,763 NC_066457 139 28 6 2 124,277 Sargassum confusum Fucales Sargassaceae NC_066460 37 25 3 2 34,719 NC_066050 139 28 6 2 124,368 Sargassum siliquastrum Fucales Sargassaceae NC_050651 37 25 3 2 34,765 NC_064337 137 28 6 2 124,529 Sargassum fusiforme Fucales Sargassaceae MN883537 37 25 3 2 34,695 MN794016 139 28 6 2 124,298 Sargassum plagiophyllum Fucales Sargassaceae NC_064731 37 25 3 2 34,862 NC_064732 139 28 6 2 124,536 Sargassum polycystum Fucales Sargassaceae NC_064729 35 25 3 0 34,825 NC_064730 139 26 6 2 124,493 Sargassum hemiphyllum Fucales Sargassaceae NC_024861 37 25 3 2 34,686 MT800998 139 28 6 2 124,319 Sargassum horneri Fucales Sargassaceae MH620963 37 24 3 2 34,621 NC_029856 139 28 6 2 124,068 Coccophora langsdorfii Fucales Sargassaceae NC_032287 37 25 3 2 35,660 NC_032288 139 27 6 2 124,450 Silvetia siliquosa Fucales Fucaceae MW485976 38 25 3 3 36,036 NC_061768 140 28 6 2 124,991 Fucus spiralis Fucales Fucaceae MG922856 37 25 3 2 36,396 MG922855 139 28 6 2 125,066 Chorda asiatica Laminariales s.l. b) Chordaceae MZ156050 40 25 3 5 41,788 MZ156037 141 28 6 0 130,274 Alaria marginata Laminariales Alariaceae NC_058764 38 25 3 3 39,389 NC_058769 141 29 6 0 130,582 Macrocystis pyrifera Laminariales Laminariaceae NC_065335 37 24 3 2 37,326 NC_065334 141 29 6 3 130,201 Saccharina japonica Laminariales Laminariaceae OP866273 38 26 3 3 37,657 OP866272 139 29 6 0 130,584 Laminaria ephemera Laminariales Laminariaceae MZ156055 38 25 3 3 37,929 MZ156035 142 29 6 1 130,610 Ectocarpus siliculosus Ectocarpales Ectocarpaceae MK045263 37 24 3 0 38,524 NC_013498 148 31 6 2 139,954 Endarachne binghamiae Ectocarpales Scytosiphonaceae NC_036747 40 23 3 5 37,460 NC_038231 143 28 6 0 136,274 Scytosiphon lomentaria Ectocarpales Scytosiphonaceae NC_025240 39 25 3 4 36,918 NC_057081 137 27 6 3 134,485 a) Mitochondrial genome annotation of Protohalopteris sp. is incomplete. b) In this study, we adopted the old classification of Laminariales, Chorda asiatica belonged to Laminariales. The single-circular mitochondrial genome (mitogenome) of P. usoehtunii is composed 32,303 bp (Fig. S2 ), similar to other Dictyotales species (31,617 − 32,021 bp, Table 1 ). The mitogenome size in Dictyotales is smaller than in all other brown algal orders, including Ralfsiales and Ishigeales (REF) (Table 1 ). The GC content of the exons and introns is, respectively, 35.40% and 40.24% (total GC content is 36.59%). The mitogenome has a high gene density (75.43%) and the conserved 36 PCGs, 25 tRNA genes, and 3 rRNA genes (Table S2 ), are commonly found in the mitogenomes of brown algae. Most of the mitogenomes have a core set of 35 genes, i.e., atp6 , atp8 , atp9 , cob , cox1 , cox2 , cox3 , nad1 , nad2 , nad3 , nad4 , ad4L , nad5 , nad6 , nad7 , nad9 , nad11 , rpl2 , rpl5 , rpl6 , rpl14 , rpl16 , rpl31 , rps2 , rps3 , rps4 , rps7 , rps8 , rps10 , rps11 , rps12 , rps13 , rps14 , rps19 and tatC . Only one Open Reading Frame (ORF) was found in P. usoehtunii , located between atp9 and rpl16 . It is also found in the other two Dictyotales, which both contain two more ORFs. In P. usoehtunii only six genes ( rpl2 , rps19 , rps3 , rpl16 , ORF121 , and tatC ) exist in the light strand with clockwise transcription direction (Fig. S2 ). Phylogenetic assessment Maximum Likelihood (ML) and Bayesian Inference (BI) trees were constructed using 115 and 35 common genes, respectively, from 27 chloroplast and 25 mitochondrial genomes (Table 1 ). The topologies of the ML and BI trees inferred from the chloroplasts and mitochondria genomes are highly congruent with maximum support values with the exception of the positions of the Desmarestiales and Fucales (Figs. 1 and 2 ). The chloroplast gene based tree showed the Dictyotales to be the sister to all other sampled orders (Fucophycidae) (Fig. 1 ), because Sphacelariales (a member of the Dictyophycidae) was assigned to the outgroup. Desmarestiales is sister to a clade comprising the other three orders in the Fucophycidae. The phylogenetic relationships based on chloroplasts genes are consistent with the results published by [ 10 ]. In contrast, in the mitochondrial gene-based tree, it is the Fucales that is sister to the other three fucophycidean orders (Fig. 2 ). Both organellar genomes demonstrated the monophyly of the Fucophycidae. Structural variation in Phaeophyceae genomes Synteny of organellar genome The chloroplast co-linearity between Padina usoehtunii (Dictyotales) and other brown algal species can help to better visualize their comparative genomic structures. The circular diagrams (Fig. 3 a) showed that the chloroplast genome of P. usoehtunii is highly conserved in structure when compared to the closely related Dictyopteris divaricata (Dictyotaceae, Dictyotales). A total of 36 co-linear blocks spanning 75,525 bp were identified, and no inversions were observed (Fig. 3 a). In comparison to Protohalopteris sp. (Sphacelariales), the co-linearity region covered 44,760 bp with 34 co-linear blocks and one identified inversion region (highlighted in gray, Fig. 3 b) spanning 30,617 bp. The co-linearity between P. usoehtunii and Desmarestia aculeata (Desmarestiales) revealed 38 co-linear blocks covering 57,426 bp, which co-linear regions are smaller than that observed in D. divaricata , but larger than that of Protohalopteris sp. (Fig. 3 c). Additionally, nine inversion regions (13,665 bp in total length) were identified in Desmarestia aculeata . The co-linearity between P. usoehtunii and five species within the order Fucales showed 29–37 co-linear blocks, spanning 37,748 to 51,710 bp (Fig. 3 d, Fig. S3 ). Notably, the co-linear regions between P. usoehtunii and most species within the order Fucales consisted predominantly of inversion regions, ranging from 24,932 to 38,959 bp. Among them, Silvetia siliquosa (C.K.Tseng & C.F.Chang) E.A.Serrão, T.O.Cho, S.M.Boo & S.H.Brawley exhibited the highest proportion of inversion regions, accounting for 76% of the co-linear sequence. In comparison to five species within the order Laminariales, the co-linearity regions ranged from 47,115 to 52,827 bp, generally larger than those observed in Fucales (Fig. 3 e, Fig. S3 ). However, the frequency of gene inversions was much lower, with only 2–5 inversion regions spanning 4,766 to 6,475 bp. When considering the co-linearity with Ectocarpales, P. usoehtunii shared the smallest co-linear regions of 39,764 bp to 47,461 bp, 17 inversion blocks covering 24,446 bp to 28,947 bp (Fig. 3 f, Fig. S3 ). Relative to the chloroplast genomes, the mitogenomes of brown algae are more conserved in structure (Fig. S4 ). Collinearity analysis of 12 brown algal mitogenomes showed that only Sphacelariales and Dictyotales underwent rearrangement, and other brown algae exhibited highly conserved mitogenomes. Mitogenome rearrangement of Dictyotales occurred in a small region, with P. usoehtunii in the range of 10,400 − 10,950 bp and Dictyopteris divaricata in the range of 10,450 − 10,980 bp, and the reset gene is atp9 . Protohalopteris sp. contained two rearrangement regions (excluding incomplete annotations), one at 2,000–2,600 bp, with nad3 and rps14 in this region; the other at 14,000–16,000 bp, with atp9 being identical to Dictyotales. Gene distribution in IR boundary region Analysis of the IR boundary regions of 25 brown algal chloroplast genes revealed a high degree of conservation in the IR region: rns , trnI , trnA , rnl , rrn5 , and rpl21 (complete or partial). Ectocarpus siliculosus also includes trnE , rpl32 , trnL , and psbA in its IR region (Fig. 1 ). However, the IR boundary regions exhibited different conservation levels. The boundary genes rns and ycf37 of the IRa region and LSC region are the most conserved, except for the species of Ectocarpales. The boundary genes between LSC and IRb are cbbx and rns in Sphacelariales, Desmarestiales, Fucales and Ectocarpales (except for E. siliculosus ), while trnL and psbY are found in species of Laminariales s.l. and Dictyotales (Fig. 1 ). The boundary genes cbbx in the Sphacelariales, Desmarestiales, and Fucales is interchangeable in genomic position with trnL in the Laminariales s.l. . Inversion of the SSC region was observed in different orders of the Phaeophyceae. The boundary and adjacent genes of the IRa and SSC regions are rpl21 and rpl3 (IRa-SSC direction) in the Dictyotales, Desmarestiales, Sphacelariales and Laminariales. The boundary and adjacent genes of IRb and SSC regions are rpl21 (except for species of Laminariales which only have one rpl21 in IRa-SSC) and ycf17 / ycf19 . Gene arrangement at the boundary of IRa-SSC and IRb-SSC regions is opposite to Ectocarpales and Fucales. Mauve collinearity analysis of chloroplast genomes of six brown algal orders showed that the entire SSC region of Dictyotales, Desmarestiales, Sphacelariales, and Laminariales species are inverted compared to those in Ectocarpales and Fucales (Fig. S5 ). Gene arrangement in mitogenome The co-linearity analysis revealed the conserved nature of brown algal mitochondrial genome structures. The arrangement of core genes, including protein-coding genes (PCGs) and rRNA as well as tRNA genes, showed that the mitochondrial PCGs consisted of the same set of 35 genes across all investigated species, except Desmarestia aculeata (Fig. 2 a). Only four genes ( atp8 , atp9 , rps10 , rpl31 ) that primarily encode components involved in ATP synthesis and ribosomal proteins exhibited variations in order across different species, with a reference to a representative species from the order Dictyotales. Additionally, Desmarestia aculeata displayed an insertion of the rpo gene in the mitogenome. These findings indicate a high degree of conservation in the types and orders of PCGs in brown algal mitogenomes. The number of tRNA genes ranged from 23 to 26 among the brown algae (Fig. 2 b). Most species possessed 25 tRNA genes, with the lowest number found in E. siliculosus (Ectocarpales) and the highest in Saccharina japonica (J.E.Areschoug) C.E.Lane, C.Mayes, Druehl & G.W.Saunders (Laminariales). Variations in tRNA gene arrangements were evident despite the relatively conserved numbers of tRNA genes. Using Padina usoehtunii as a reference, the most common changes in tRNA gene positions occurred in trnK (excluding Dictyota dichotoma ), trnE , trnD and trnA (excluding Dictyotales). In most cases, changes in the positions of trnA and trnD were linked. In Laminariales, the position of trnA - trnD occurred between trnS1 - trnY2 / trnS2 . The variability in the trnE position was typically situated between trnI and trnK . Sequences variation in Phaeophyceae genomes Base evolutionary rate Non-synonymous (dN) and synonymous (dS) substitution rates across 24 brown algal species encompassing five orders (Tables S3, S4) can help to understand sequence variations of chloroplast and mitochondrial common PCGs. Among the 115 chloroplast genes, the highest dN value was observed in rps20 (0.3385), while the lowest values were found in petN and psbL (0.0001). The photosystem II genes psbA , psbE , and psbK exhibited the lowest dS (0.3506–0.3770) and relatively small dN values (0.0138–0.0518). The dN/dS ratios were smallest for petN (0.0001 < < 1) and psbL (0.0002 < < 1) (Fig. S6 a), indicating an intense purifying selection. Conversely, the genes petF and rpl9 displayed the highest dN/dS ratios (0.4401 < 1, 0.3960 < 1), indicating a weak purifying selection. The dN/dS ratios for major functional gene categories, including ATP synthesis, photosystem, cytochrome b/f complex, chlorophyll biosynthesis and ribosomal proteins, revealed significant differences across these five functional groups ( p = 0.001) (Fig. 4 a). Specifically, ribosomal proteins exhibited significant differences in dN/dS ratios compared to genes involved in photosystem, light harvesting and chlorophyll biosynthesis ( p = 0.001, p = 0.009). The highest average dN/dS ratio (0.1595) in ribosomal proteins indicates a much weak evolutionary pressure. The lowest average dN/dS ratios (0.0626, 0.0632) detected in genes involved in light harvesting, chlorophyll biosynthesis and photosystem categories suggest the strongest purifying selection. Among the 35 mitochondrial genes, the highest dN/dS ratio occurred in ribosomal protein genes: rpl5 (0.2825), rps10 (0.2853), rps11 (0.2952), rps2 (0.3071), and rpl31 (0.4309) (Fig. S6 b, Table S4 ), suggesting their relatively accelerated evolutionary rates. The lowest ratio was found in atp9 (0.0168). The dN/dS ratios for four functional groups in mitogenome (ATP synthase, cytochrome c oxidase, NADH dehydrogenase and ribosomal proteins) (Fig. 4 b), detected significantly high values in ribosomal protein genes compared to cytochrome c oxidase ( p = 0.009) and NADH dehydrogenase genes ( p = 0.001). Significant differences in dN and dS values were observed between the mitochondrial genes and chloroplast genomes of brown algae ( p = 0.001). The dN values of chloroplast genes ranged from 0.0001 to 0.3385, whereas those of mitochondria ranged from 0.0062 to 0.4213 (Tables S3-S4). The dS values of chloroplast genes ranged from 0.3506 to 1.1051, whereas the mitochondrial ones ranged from 0.9423 to 2.0364 (except atp9 , dS = 0.3697). Most mitochondrial genes generally showed higher dS and dN values than the chloroplast genes (Fig. 5 ), indicating that mitochondrial genes had higher mutation rates than the chloroplast genes in brown algae. The dN/dS values of chloroplast genes ranged from 0.0098 to 0.4401 (except petN (dN/dS = 0.0001) and psbL (dN/dS = 0.0002)) and those of mitochondrial genes ranged from 0.0168 to 0.4309 (Fig. S6 ). This statistically non-significant difference ( p = 0.724) manifests that they both experienced purifying selection at similar levels. Codon usage RSCU values revealed the use preferences of 61 codons (excluding three stop codons) in brown algae. AUU was the most frequent codon for Leu in chloroplast and mitochondrial genomes. Approximately 25–27 codons (RSCU > 1) were preferred in organellar genomes. RSCU > 1.6 is considered as over-preference for codons, while RSCU 1.6, average RSCU = 2.00) whereas 27 codons were underused (RSCU 1.6, average RSCU = 2.26) and eight under-preferred codons (RSCU < 0.6, average RSCU = 0.30) (Fig. S8 ). The codon bias of the chloroplast genome is stronger than that of the mitogenome in brown algae and the third position of frequently used codons was predominantly A or U. Repeat sequences A total of 105 ( Padina usoehtunii ) to 157 ( Chorda asiatica Sasaki & Kawai) simple sequence repeats (SSRs) were detected in 14 chloroplast genomes, including 81–113 mononucleotides (mono-), 4–16 dinucleotides (di-), 3–13 trinucleotides (tri-), 4–15 tetranucleotides (tetra-), 0–5 pentanucleotide (penta-), and 0–2 hexanucleotide (hexa-) (Fig. S9 ). In 14 mitogenomes analyzed, there are 22 ( P. usoehtunii ) to 52 ( E. siliculosus and Scytosiphon lomentaria (Lyngbye) Link) SSRs, and the numbers of mono-, di-, tri-, tetra-, penta-, and hexa-nucleotide are 20–47, 0–3, 0–2, 0–4, 0–1, 0–1, respectively (Fig. S9 ). The most numerous mononucleotides repeats are of the A and T type. P. usoehtunii had the least numbers of SSRs among brown algae. We identified the forward (F), reverse (R), palindromic (P), and complementary (C) repeat sequences in chloroplast and mitochondrial genomes of brown algae (Fig. 6 ). Palindromic repeats are the most frequent in chloroplast genomes, while forward repeats are the most frequent type in mitogenomes. Complementary repeats are the least frequent type in both organelle genomes. The amount of these long repeat sequences was highly variable in mitogenomes, with 38 forward repeats and 6 palindromic repeats in Protohalopteris sp., 20 forward repeats and 15 palindromic repeats in P. usoehtunii . In chloroplast genomes, the numbers of different repeat types is more conservative within the same brown algal order. Discussion When codon bias, number and types of repeat sequences, and particularly genome size and structure, were mapped on the phylogenetic tree of the Phaeophyceae, varying degrees of diversity at the order level became apparent (Figs. 1 and 2 ). The structural differences in chloroplast genome primarily reflected on the size and types of genes at the IR boundary region and the rearrangement of the SSC region, which may mechanically be related to gene replication. In brown algae, chloroplast genomes are more variable in structure, while mitochondrial genomes exhibit higher sequence variation. This pattern is similar in red algae [ 28 , 29 ], but contrasts that in land plants and green algae [ 30 ]. The rate of sequence evolution is likely influenced by the extent of organellar genome modification as observed in terrestrial plants [ 31 ]. Organelle genome size and gene loss The Dictyotales with divergence time around 155 Ma [ 5 ] has a smaller chloroplast genome size, compared to later divergence clades within the BACR clade, except Fucales (Fig. 1 ), which has a similar chloroplast genome size as Dictyotales (around 125 kb). Previous researches showed a positive correlation between chloroplast genome size and the total length of non-coding sequences [ 32 ], suggesting that the accumulation of non-coding regions contributes to larger chloroplast genomes, possibly facilitating the emergence of new genes. In comparison with other orders of Phaeophyceae, Dictyotales exhibits distinctive gene losses in its chloroplast genome: rbcR and rpl32 (Fig. S1 ). RbcR is a potential transcriptional regulator of Rubisco and its absence has not been observed in other brown algal lineages. Horizontal gene transfer likely occurred between the organelles and the nucleus in Dictyotales, leading to the presence of rbcR in the nucleus [ 33 ]. This hypothesis requires further validation. Rpl32 has been found to be lost in 21 algal chloroplast genomes, mostly belonging to the Streptophyta, like some seed plants: eudicots, gymnosperms, magnoliids, and monocots [ 34 ]. Gene loss events within chloroplast genomes have been observed in other Ochrophyta lineages such as Dictyochophyceae and Synurophyceae [ 35 , 36 ], suggesting that these gene loss events are not uncommon during the course of evolution. The loss of rbcR and rpl32 genes happened after the SSDO-BACR split, because secondary gain of these genes in the BACR clade is highly unlikely. We do not know whether these genes were lost early during SSDO evolution or whether it happened later, because no SSDO chloroplasts other than those from the Dictyotales have been sequenced. Variation of organelle genome structure Structural comparison of chloroplast genomes between Padina usoehtunii and other orders revealed clear differences across the phylogenetic tree of brown algae. The BACR orders Laminariales, Fucales, and Desmarestiales showed large structural differences compared to Dictyotales in chloroplast genome organization (Fig. S3 ). Notably, Dictyotales displayed a smaller number of inverted regions compared to the Laminariales than to the Fucales and Ectocarpales (Fig. S3 ). A certain degree of chloroplast genome structural instability can generate adaptive and recovery mechanisms to cope with environmental changes, accelerating the evolutionary trajectory of brown algae and aiding their expansion into a wide range of geographical environments [ 37 ]. The IR region is crucial in terrestrial plants as it stabilizes chloroplast genome organization, mediates intramolecular recombination, and increases the copy number of rRNA genes [ 38 ]. The expansion and contraction of the IR region are linked to the addition or reduction of boundary genes (Fig. 2 ). The size of the IR region varies significantly among different Ochrophyta algae, such as Raphidophyceae and Bacillariophyceae, which have IR sizes of 18–22 kb, approximately three times larger than that in brown algae (5–9 kb). The IR region in brown algae includes rRNA and tRNA genes, while in the Raphidophyceae and Bacillariophyceae it also contains ribosomal protein genes such as rpl32 , rpl21 , rpl34 , as well as photosystem II genes psbA , psbY , and psbC [ 39 , 40 ]. The IR region structure in oogamous (with maternal chloroplast inheritance) Dictyotales, Laminariales, and Fucales, is relatively conserved, while substantial structural variation is observed among different species of isogamous Ectocarpales (with biparental chloroplast inheritance), which accumulate more variation compared to oogamous brown algae, leading to a higher rate of structural rearrangements [ 32 ]. Rpl21 is a common gene between the IR and SSC boundary regions in brown algae. The contraction or expansion of the IR region can affect the location of rpl21 (Fig. 1 ). When the IR region is large, the rpl21 gene and its replicates are present in the IRa and IRb, as in the Dictyotales (IR: 5.8-6 kb), Sphacelariales (IR: 5.9 kb), and Ectocarpales (IR: 5.5–8.6 kb). When the IR region is small, rpl21 will span the IR and SSC regions, as in the Desmarestiales (IR: 5.3 kb), Fucales (IR: 3.4–5.4 kb), and Laminariales (IR: 5.4–5.5 kb). The inversion of the entire SSC region happened two times, the first occurred between 144.6–54.6 Ma, after the split of the Fucales from the Desmarestiales, and the second occurred between 125.0-51.5 Ma, after the split of the Ectocarpales from the Laminariales s.l. . (Fig. S5 ) [ 5 ]. This extensive inversion might have arisen due to the replication mechanisms, such as recombination-dependent replication (RDR). During replication, invasions mediated by reverse repeats in the plastid genome result in gene conversion carried out through unidirectional crossovers, thereby giving rise to single-copy region inversions [ 37 ]. Phylogenetic analysis showed that the cbbx gene originated in cyanobacteria [ 33 ]. The CbbX protein can function as an activase of inhibited red-type Rubisco [ 41 ]. cbbx in the brown alga Saccharina japonica has been reported to exist in the nuclear and in the chloroplast genome [ 41 ]. The nuclear-encoded cbbx ( cbbx-n ) exhibits higher enzyme activity compared to the plastid-encoded cbbx ( cbbx-p ). Cbbx-n can interact with cbbx-p to form a heterohexamer, promoting higher catalytic efficiency of Rubisco, thereby accelerating the rate of carbon assimilation in photosynthesis. The rearrangements of the cbbx gene in certain brown algal lineages may affect the catalyzing efficiency of Rubisco, thus influencing the rate of carbon assimilation in photosynthesis. However, this hypothesis requires further experimental validation. Variation of organellar genome sequence We found a significantly higher non-synonymous (dN) substitution rate in mitochondrial genes compared to chloroplast genes, which is consistent with the previous research on the evolutionary rate in brown algae [ 18 ]. The average synonymous (dS) substitution rate in mitochondria is higher than in chloroplasts, although this distinction is not clearly discernible in the scatterplot in Fig. 5 . This observation may be attributed to the inclusion of Dictyotales and Sphacelariales. Nevertheless, when considering the entire organellar genome dataset, it is evident that brown algal mitochondrial genes have a faster mutation rate than chloroplasts genes (Table S3 - S4 ). This was also observed in the phytoplankton Phaeocystis (Haptophyta) and the red alga Porphyra [ 42 , 43 ], but this trend was in contrast to most land plants, where the dS value of mitochondria were three times lower than the chloroplasts [ 44 ]. For both chloroplast and mitochondrial genomes, the average dN/dS values for all protein coding genes (PCGs) are less than 1, suggesting that these genes have undergone purifying selection. However, genes from different functional categories showed variable dN/dS values. Notably, the ribosomal protein genes, whether in chloroplasts or in mitochondria, exhibited the highest average dN/dS values, suggesting a much weaker purifying selection on it. In the chloroplast genomes, the strongest purifying selection is observed in the photosystem genes, consistent with the predicted dN/dS values for the primary functional groups of 23 brown algal species reported recently [ 18 ]. These differences of the dN/dS values with different function genes reflected variation in the strength of purifying selection. Highly preferred codons in both chloroplast and mitochondrial genomes all ended with A/U, while less preferred codons ended with C/G (Figs. S7-S8). Codon preference analysis indicates that codon usage patterns are similar among different brown algal species. However, codon bias in the brown algal chloroplast genome is higher than in the mitochondrial genome. Selective pressure and gene mutations are likely important factors to influence codon usage [ 45 ], possibly due to the high AT content in organellar genomes which can potentially lead to a bias towards AU in codons. Next, sequencing more organellar genome of representative taxon can largely contribute to the understanding of the structural genomics and molecular evolution of the brown algal tree of life. Materials and methods Sample collection and DNA extraction Padina usoehtunii was collected from the intertidal at Pakarang Cape (8º44'17.9"N 98º13'05.5"E) in Phang-nga province on the Andaman coast of Thailand in December 2019, silica-dried and transported to Qingdao, China. Species identification was a posteriori confirmed by comparing mitocondrial cox 1 and chloroplast-encoded rbc L gene sequences to the representative DNA sequences of the P. usoehtunii type specimen (Genbank AB512597 and AB512559, respectively). The total DNA was extracted from young thallus using the FastPure® Plant DNA Isolation Mini Kit (Vazyme Biotech Co., China). The extracted DNA was purified using a DNA Purification Kit (Vazyme Biotech Co., China) according to manufacturer’s instructions. Genome sequencing, assembly and annotation To obtain full-length chloroplast and mitochondria genome sequences, we used the paired-end (Illumina Hiseq) strategy in this study. First, approximately 1 µg of purified DNA was made into libraries using the TruSeq™ Nano DNA Sample Prep Kit from Illumina according to the manufacturer’s protocol. Libraries were sequenced using an Illumina Hiseq 4000 with 150 bp paired-end reads length (Biozeron, Shanghai, China). The raw reads were checked with FastQC and trimmed by Trimmomatic-0.39 [ 46 ]. Algal organellar genomes assembly was performed using NOVOPlasty v2.7.2 software ( https://github.com/ndierckx/NOVOPlasty ). The near-source reference genome was used as the seed sequence, with the remaining parameters set as default. Clean reads were compared back on the Scaffold obtained by assembly, and based on the paired-end and overlap of reads, the assembly results were partially assembled and optimized. GapCloser v1.12 ( http://soap.genomics.org.cn/soapdenovo.html ) was used to repair the internal holes in the assembly. The mitochondrial and chloroplast genes were annotated using the online GeSeq tool ( https://chlorobox.mpimp-golm.mpg.de/geseq.html/ ) to predict protein coding genes, tRNA and rRNA, using following parameters: Protein search identity: 60; rRNA, tRNA, DNA search identity: 35; 3rd Party tRNA annotators: tRNAscan-SE. The position of each coding gene was determined using BLAST [ 47 ] searches against reference genes. Manual corrections of genes for start/stop codons and for intron/exon boundaries were performed in SnapGene Viewer. The circular maps of genomes were displayed using the software OGDRAW ( https://chlorobox.mpimp-golm.mpg.de/OGDraw.html ). Gene function annotation was performed with available protein databases by BLASTp (evalue ≤ 10 − 5 ), including NCBI Non-Redundant Protein Sequence Database (NR), Swiss-Prot, Clusters of Orthologous Groups (COGs), and Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) terms. Finally, we submitted the mitochondrial and chloroplast genomes of Padina usoehtunii to the GenBank database with accession numbers MW485979 and MW485982, respectively. Phylogenetic analysis We selected 27 and 25 species from 6 orders of Phaeophyceae (Table 1 ) to construct mitochondrial and chloroplast phylogenetic trees respectively, using Protohalopteris sp. (Sphacelariales) as outgroup. Sequences of 35 and 115 shared genes from mitogenomes and chloroplast genomes were aligned by mafft v7.313 [ 48 ] and the sequences were corrected with Gblock 0.91b [ 49 ]. IQtree v.1.6.8 [ 50 , 51 , 52 ] and MrBayes 3.2.6 [ 53 ] were used to construct Maximum likelihood (ML) and Bayesian inference (BI) trees, respectively. ModelFinder [ 54 ] was used to select the best nucleotide substitution model based on Akaike information criterion (AIC). The best-fit models GTR + F + I + G4 (G = 0.232, I = 0.800) and GTR + F + I + G4 (G = 0.352, I = 0.853) were used for mitochondria and chloroplast, respectively. For ML tree construction, the parameters were set to 1000 ultrafast bootstrap replicates with others as default [ 55 ]. For BI tree, the Markov Chain Monte Carlo (MCMC) were set to 1×10 6 generations running with a tree sampling frequency of every 1000 generations and the first 25% was discarded as burn-in. Finally, FigTree v1.4.4 ( http://tree.bio.ed.ac.uk/software/figtree/ ) was used to beautify the tree files. Genome synteny and IR boundary regions analysis We used TBtools v1.108 to map the collinearity of chloroplast genome structure between P. usoehtunii and six species from the Dictyotales, Sphacelariales, Desmarestiales, Laminariales, Ectocarpales, and Fucales, respectively [ 56 ]. The species annotation order was manually adjusted to be consistent to ensure correct collinear correspondence. BLAST [ 47 ] was used to match synteny, sequences with less than 100 bp were removed, and only a pair of IR collinear information (IRa-IRa, IRb-IRb) was retained. Mauve [ 57 ] was used to detect linear collinearity of chloroplast genomes, setting to align with progressive Mauve. In order to explore the differences of chloroplast LSC/IR/SSC region boundaries, we plotted the genes between each partition by CPJSdraw v1.0.0 [ 58 ]. Base substitution rate estimation To explore evolutionary rates of brown algal organelle genomes, we extracted 35 and 115 shared PCGs from 24 species whose both organelles have been sequenced using PhyloSuite v1.2.2 [ 59 ]. The genome datasets of Phaeophyceae were obtained from GenBank (Table 1 ). MAFFT [ 60 ] and Gblocks [ 61 ] were used for sequence alignment and correction, respectively. The aligned sequence was converted into pml format by PhyloSuite v1.2.2 [ 59 ]. We used PAML v4.10 [ 62 ] to estimate non-synonymous (dN) and synonymous substitution (dS) of 24 mitogenomes and chloroplast genomes. The parameters set to runmode = 0 and CodonFreq = 2. To avoid data bias we calculated the median pairwise comparisons data of each gene. The histogram was drawn to show dN/dS values of each gene. The scatter plot was drawn to show the tendency of differences in dN/dS values among chloroplasts and mitochondria. We used the Kruskal-Wallis test in SPSS v26.0 software (IBM, Armonk, NY, USA) to explore the diversity in dN/dS values of different functional genes. The comparison of substitution rate between the two organelles was also tested using the method above. Repeat sequences and codon preference analysis Short Sequence Repeats (SSRs) were identified using MISA [ 63 ]. The parameter settings were as follows: mono-, di-, tri-, tetra-, pent-, and hexa-nucleotide motifs have at least 8, 5, 4, 3, 3 and 3 repeats, respectively. We used REPuter ( http://bibiserv.techfak.uni-bielefeld.de/reputer ) to detect forward (F), palindromic (P), reverse (R) and complementary (C) repeats with Hamming distance equal to 3 and minimum repeat size of 20 bp [ 64 ]. The PCGs of organelles were extracted by PhyloSuitev1.2.2 [ 59 ]. CodonW1.4.4 [ 65 ] was used to calculate the relative synonymous codon usage (RSCU) of each PCGs. RSCU = 1 means no bias in codon usage. RSCU 1 shows more preference in codon usage [ 66 ]. Abbreviations AIC: Akaike information criterion; BACR: Brown algal crown radiation; BI: Bayesian inference; Cbbx -n: Nuclear-encoded cbbx; Cbbx -p: Plastid-encoded cbbx; COGs: Clusters of Orthologous Groups; dN: Non-synonymous substitution; dS: Synonymous substitution; GO: Gene Ontology; IR: Inverted repeat; ITS: Internal transcribed spacer; KEGG: Kyoto Encyclopedia of Genes and Genomes; LSC: Long single copy; Ma: Mega-annum; MCMC: Markov Chain Monte Carlo; ML: Maximum likelihood; NR: Non-Redundant Protein Sequence Database; ORF: Open Reading Frame; PCGs: Protein coding genes; RDR: Recombination-dependent replication; rRNAs: Ribosomal RNA genes; SSC: Short single copy; SSDO: Sphacelariales, Syringodermatales, Dictyotales, and Onslowiales; tRNAs: Transfer RNA genes; Declarations Data Availability The datasets used in this study are entirely included in the article and supplementary files. Availability and usage of the datasets require the consent of the corresponding author. The GenBank accession numbers of the chloroplast and mitochondrial genomes of Padina usoehtunii are MW485982 and MW485979, respectively. The chloroplast and mitochondrial genomes data of other brown alga were obtained from NCBI. Acknowledgements We are grateful for the joint support from the National Natural Science Foundation of China (32371697), the National Natural Science Foundation of China (41761144057) and the Thailand Research Fund (RDG6130002). Authors’ contributions Zi-Min Hu and Stefano G. A. Draisma led this project. Yi-Jia Liu, Tong-Yun Zhang and Qi-Qi Wang collectively conducted the experiments and performed data analysis. Yi-Jia Liu drafted the manuscript. Zi-Min Hu provides important advice on writting. Stefano G. A. Draisma collected the samples and revised the manuscript. All authors approved the final version of the manuscript for publication. Funding This work was supported by National Natural Science Foundation of China (32371697), a joint research grant between National Natural Science Foundation of China (41761144057) and Thailand Research Fund (RDG6130002). Ethics approval and consent to participate Not applicable. Sample collection permission The field collection of seaweed samples in this article complies with the relevant Thailand and international guidelines/regulations/ legislation. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Author details 1 Ocean School, Yantai University, Yantai 264005, China. 2 Excellence Center for Biodiversity of Peninsular Thailand, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90110, Thailand. References Kurland CG, Andersson SG. Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev. 2000;64(4):786–820. Kutschera U, Niklas KJ. Endosymbiosis, cell evolution, and speciation. Theory Biosci. 2005;124(1):1–24. Brindefalk B, Ettema TJ, Viklund J, Thollesson M, Andersson SG. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS ONE. 2011;6(9):e24457. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature. 2010;465:617–21. Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the brown algal crown radiation. Mol Phylogenet Evol. 2010;56(2):659–74. Rajanikanth A. A fossil marine brown alga from the Gangapur Formation, Pranhita-Godavari Graben. Curr Sci. 1989;58(2):78–80. Parker BC, Dawson EY. Non-calcareous marine algae from California Miocene deposits. Nova Hedwigia Beihefte. 1965;10:273–95. Reviers BD, Rousseau F. Towards a new classification of the brown algae. Phycol Res. 1999;13(1):107–201. Draisma SGA, van Prud'homme WF, Stam WT, Olsen JL. A reassessment of phylogenetic relationships within the Phaeophyceae based on Rubisco large subunit and ribosomal DNA sequences. J Phycol. 2001;37(4):586–603. Bringloe TT, Starko S, Wade RM, Vieira C, Kawai H, Clerck OD, et al. Phylogeny and evolution of the brown algae. Crit Rev Plant Sci. 2020;39(4):281–321. Wei L, Xin Y, Wang D, Jing X, Zhou Q, Su X, et al. Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. BMC Genomics. 2013;14:534. Muhlin JF, Brawley SH. Recent versus relic: discerning the genetic signature of Fucus vesiculosus (Heterokontophyta; Phaeophyceae) in the Northwestern Atlantic. J Phycol. 2009;45(4):828–37. Hu ZM, Uwai S, Yu SH, Komatsu T, Duan DL. Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol. 2011;20(18):3894–909. Hu ZM, Kantachumpoo A, Liu RY, Sun ZM, Yao JT, Komatsu T, Uwai S, Duan DL. A late Pleistocene marine glacial refugium in the south-west of Hainan Island, China: phylogeographical insights from the brown alga Sargassum polycystum . J Biogeogr. 2018;45:355–66. Li JJ, Hu ZM, Sun ZM, Yao JT, Liu FL, Fresia P, Duan DL. Historical isolation and contemporary gene flow drive population diversity of the brown alga Sargassum thunbergii along the coast of China. BMC Evol Biol. 2017;17:246. Montecinos AE, Couceiro L, Peters AF, Desrut A, Valero M, Guillemin ML. Species delimitation and phylogeographic analyses in the Ectocarpus subgroup siliculosi (Ectocarpales, Phaeophyceae). J Phycol. 2017;53(1):17–31. Chen J, Zang Y, Liang S, Xue S, Shang S, Zhu M, et al. Comparative analysis of mitochondrial genomes reveals marine adaptation in seagrasses. BMC Genomics. 2022;23(1):800. Starko S, Bringloe TT, Gomez MS, Darby H, Graham SW, Martone PT. Genomic rearrangements and sequence evolution across brown algal organelles. Genome Biol Evol. 2021;13(7):evab124. Liu F, Pan J, Zhang Z, Zhang ZS, Moejeset FW. Organelle genomes of Sargassum confusum (Fucales, Phaeophyceae): mtDNA vs cpDNA. J Appl Phycol. 2018;30:2715–22. Zhang SS, Liang YS, Zhang J, Draisma SGA, Duan D. Organellar genome comparisons of Sargassum polycystum and S. plagiophyllum (Fucales, Phaeophyceae) with other Sargassum species. BMC Genomics. 2022;23(1):629. Vieira C, Steen F, D’hondt S, Bafort Q, Tyberghein L, Fernandez-García C, et al. Global biogeography and diversification of a group of brown seaweeds (Phaeophyceae) driven by clade-specific evolutionary processes. J Biogeogr. 2021;48:703–15. Vieira C, Camacho O, Sun Z, Fredericq S, Leliaert F, Payri C, et al. Historical biogeography of the highly diverse brown seaweed Lobophora (Dictyotales, Phaeophyceae). Mol Phylogenet Evol. 2017;110:81–92. Guiry MD, Guiry GM. 2023. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org ; searched on December 22, 2023. Ni-Ni-Win, Hanyuda T, Arai S, Uchimura M, Prathep A, Draisma SGA et al. A taxonomic study of the genus Padina (Dictyotales, Phaeophyceae) including the descriptions of four new species from Japan, Hawaii, and the Andaman sea. 2011;47(5):1193–209. Wichachucherd B, Prathep A. Preliminary study on the diversity and distribution of Padina Adanson in Peninsular Thailand, including a new record, Padina usoehtunii Ni-Ni-Win et Kawai. Inst Ocean Earth Sci Univ Malaya Monogr. 2013;15:175–83. Wichachucherd B. Phylogeography of Padina boryana (Dictyotales, Phaeophyceae) around the Thai-Malay Peninsula. Ph.D. dissertation Prince of Songkhla University, Hat Yai, Thailand. 2014;57 pp. Deb B, Uddin A, Chakraborty S. Composition, codon usage pattern, protein properties, and influencing factors in the genomes of members of the family Anelloviridae. Arch Virol. 2021;166(2):461–74. Kim H, Yang JH, Bustamante DE, Calderon MS, Mansilla A, Maggs CA, et al. Organelle genome variation in the red algal genus Ahnfeltia (Florideophyceae). Front Genet. 2021;12:724–34. Lee JM, Song HJ, Park SI, Lee YM, Jeong SY, Cho TO, et al. Mitochondrial and plastid genomes from coralline red algae provide insights into the incongruent evolutionary histories of organelles. Genome Biol Evol. 2018;10(11):2961–72. Smith DR. Mutation rates in plastid genomes: they are lower than you might think. Genome Biol Evol. 2015;7(5):1227–34. Smith DR, Keeling PJ. Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc. Natl Acad Sci U S A. 2015;112(33):10177–10184. Choi JW, Graf L, Peters AF, Cock JM, Nishitsuji K, Arimoto A, et al. Organelle inheritance and genome architecture variation in isogamous brown algae. Sci Rep. 2020;10(1):2048. Maier UG, Fraunholz M, Zauner S, Penny S, Douglas S. A nucleomorph-encoded CbbX and the phylogeny of RuBisCo regulators. Mol Biol Evol. 2000;17(4):576–83. Mohanta TK, Khan A, Khan AL, Hashem A, Abd_Allah EF, Al-Harrasi A. Gene Loss and Evolution of the Plastome. Genes. 2020;11(10):1133. Han KY, Maciszewski K, Graf L, Yang JH, Andersen RA, Karnkowska A, et al. Dictyochophyceae plastid genomes reveal unusual variability in their organization. J Phycol. 2019;55(5):1166–80. Kim JI, Shin H, Škaloud P, Jung J, Yoon HS, Archibald JM, et al. Comparative plastid genomes of Synurophyceae: inverted repeat dynamics and gene content variation. BMC Evol Biol. 2019;19(1):20–33. Maréchal A, Brisson N. Recombination and the maintenance of plant organelle genome stability. New Phytol. 2010;186(2):299–317. Goulding SE, Olmstead RG, Morden CW, Wolfe KH. Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet. 1996;252(1–2):195–206. Cattolico RA, Jacobs MA, Zhou Y, Chang J, Duplessis M, Lybrand T, et al. Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics. 2008;9:211. Lommer M, Roy AS, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J. Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genomics. 2010;11:718. Bi YH, Feng B, Xie WY, Ouyang LL, Ye RX, Zhou ZG. Nuclear-encoded CbbX located in chloroplast is essential for the activity of red-type Rubisco in Saccharina japonica . Plant Physiol Biochem. 2023;196:236–45. Smith DR, Arrigo KR, Alderkamp AC, Allen AE. Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of Phaeocystis algae. Mol Phylogenet Evol. 2014;71:36–40. Smith DR, Hua J, Lee RW, Keeling PJ. Relative rates of evolution among the three genetic compartments of the red alga Porphyra differ from those of green plants and do not correlate with genome architecture. Mol Phylogenet Evol. 2012;65:339–44. Drouin G, Daoud H, Xia J. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol. 2008;49:827–31. Wang H, Meng T, Wei W. Analysis of synonymous codon usage bias in helicase gene from Autographa californica multiple nucleopolyhedrovirus. Genes Genom. 2018;40(7):767–80. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56(4):564–77. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21. Minh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30:1188–95. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9. Minh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30(5):1188–95. Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202. Darling AC, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394–403. Li H, Guo Q, Xu L, Gao H, Liu L, Zhou X. CPJSdraw: analysis and visualization of junction sites of chloroplast genomes. PeerJ. 2023;11:e15326. Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, et al. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 2020;20(1):348–55. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56(4):564–77. Yang Z. PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24(8):1586–91. Beier S, Thiel T, Münch T, Scholz U, Mascher M. MISA-web: a web server for microsatellite prediction. Bioinformatics. 2017;33(16):2583–5. Kurtz S, Schleiermacher C. Reputer: fast computation of maximal repeats in complete genomes. Bioinformatics. 1999;15(5):426–7. Peden JF. Analysis of codon usage. Univ Nottm. 2000;90(1):73–4. Behura SK, Severson DW. Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS ONE. 2012;7(8):e43111. Additional Declarations No competing interests reported. Supplementary Files FigureS1.pdf Fig S1.Gene circle map of the complete chloroplast genome of Padina usoehtunii . FigureS2.pdf Fig S2.Gene circle map of the complete mitochondrial genome of Padina usoehtunii . FigureS3.pdf Fig S3.Synteny circular diagrams comparing the chloroplast genome of Padina usoehtunii with those of representatives of the Laminariales s.l. (p.1), Ectocarpales (p.2), and Fucales (p.3). FigureS4.pdf Fig S4. The collinearity analysis of mitochondrial genomes of 12 brown algal species representing 6 orders. FigureS5.pdf Fig S5.The collinearity analysis of chloroplast genomes of species from 5 brown algal orders. Yellow-marked areas indicate the short single copy (SSC) regions. FigureS6.pdf Fig S6.Chloroplast (a) and mitochondrial (b) genes nonsynonymous to synonymous substitution ratios (dN/dS) among 24 selected Phaeophyceae species. FigureS7.pdf Fig S7. Relative synonymous codon usage (RSCU) in the chloroplast genomes of 6 orders in the Phaeophyceae. FigureS8.pdf Fig S8.Relative synonymous codon usage (RSCU) in the mitochondrial genomes of 6 orders in the Phaeophyceae. FigureS9.pdf Fig S9. Numbers of different short sequence repeat (SSR) types detected in chloroplast (a) and mitochondrial (b) genomes of 14 brown algae. TableS1.docx TableS2.docx TableS3.docx TableS4.docx Cite Share Download PDF Status: Published Journal Publication published 31 Jul, 2024 Read the published version in BMC Genomics → Version 1 posted Editorial decision: Revision requested 06 Feb, 2024 Reviews received at journal 03 Feb, 2024 Reviewers agreed at journal 23 Jan, 2024 Reviewers invited by journal 23 Jan, 2024 Editor assigned by journal 19 Jan, 2024 Editor invited by journal 09 Jan, 2024 Submission checks completed at journal 09 Jan, 2024 First submitted to journal 04 Jan, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3835960","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":266085036,"identity":"9390cd65-7455-46f7-9d97-92591d4591da","order_by":0,"name":"Yi-Jia Liu","email":"","orcid":"","institution":"Yantai University","correspondingAuthor":false,"prefix":"","firstName":"Yi-Jia","middleName":"","lastName":"Liu","suffix":""},{"id":266085037,"identity":"338581e2-49f9-46cb-863c-f4e047e0a814","order_by":1,"name":"Tong-Yun Zhang","email":"","orcid":"","institution":"Yantai University","correspondingAuthor":false,"prefix":"","firstName":"Tong-Yun","middleName":"","lastName":"Zhang","suffix":""},{"id":266085038,"identity":"93f0d2c5-cad9-45c7-a1ca-7b7f7e29606a","order_by":2,"name":"Qi-Qi Wang","email":"","orcid":"","institution":"Yantai University","correspondingAuthor":false,"prefix":"","firstName":"Qi-Qi","middleName":"","lastName":"Wang","suffix":""},{"id":266085039,"identity":"b46bf985-d0c5-4d37-bc2b-d64dab528448","order_by":3,"name":"Stefano G.A. Draisma","email":"","orcid":"","institution":"Prince of Songkla University","correspondingAuthor":false,"prefix":"","firstName":"Stefano","middleName":"G.A.","lastName":"Draisma","suffix":""},{"id":266085040,"identity":"63495231-5983-4f6a-8687-ea0e3aa04e8c","order_by":4,"name":"Zi-Min Hu","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA1ElEQVRIiWNgGAWjYBACAyA+ACTl7A8zH3yQUFFDvBZjhuNsyQYPzhwjTgsIJDac5zGTfNjCTFiLuUT6w0M3Cu4kNjYzmFUkNrAx8Ld3J+DVYjkjIeFwjsEz42ZmhrQbiTtkGCTOnN2A32E3Eg4AtRyWbWNmOHYj8Qwbg4FELiEtiQ0gLYw9zIxtBYlAjURoSWYAaVGcwczMxkCcljPPwFqMDZjZmCUSzhzjIeyX4+mPP+f8OSxnwH/+48cfFTVy/O29+LVgAB7SlI+CUTAKRsEowAoAkfBNRIphJQkAAAAASUVORK5CYII=","orcid":"","institution":"Yantai University","correspondingAuthor":true,"prefix":"","firstName":"Zi-Min","middleName":"","lastName":"Hu","suffix":""}],"badges":[],"createdAt":"2024-01-05 02:44:10","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3835960/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3835960/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12864-024-10616-4","type":"published","date":"2024-07-31T15:57:56+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":49465691,"identity":"aa38e0af-5433-4003-81c2-2ab43e74819b","added_by":"auto","created_at":"2024-01-11 09:35:29","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":860391,"visible":true,"origin":"","legend":"\u003cp\u003ePhylogenetic tree of brown algae (outgroup=Sphacelariales) constructed using the 115 shared chloroplast PCGs with IR, LSC, and SSC gene arrangement in boundary regions. The Maximum likelihood bootstrap support values and Bayesian posterior probabilities of all nodes are 100 and 1, respectively. The numbers before the tree nodes represent the mean divergence times retrieved from Silberfeld et al. (2010). Schematic representations of the chloroplast genomes for each taxon are shown right from the tree. Arrow icons of the same color represent the same genes, with arrow direction indicating the transcription orientation. Adjacent to boundary genes are represented by dashed line icons.\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/3efa48aae434db2a96fddc4b.png"},{"id":49464985,"identity":"ae20f283-c580-4e03-aa56-938e487e963b","added_by":"auto","created_at":"2024-01-11 09:27:30","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":743172,"visible":true,"origin":"","legend":"\u003cp\u003eArrangement order of PCGs (a) and tRNAs (b) in mitochondrial genomes with the cladogram of brown algae constructed using the 35 shared mitochondrial PCGs (b).\u003cem\u003e \u003c/em\u003eMost nodes had high support values, except for the marked numbers nodes\u003cem\u003e. \u003c/em\u003eUsing the \u003cem\u003ePadina usoehtunii \u003c/em\u003emitogenome\u003cem\u003e \u003c/em\u003eas reference (yellow squares), other color squares represent changed genes, dashed square represent inserted genes, solid squares represent replaced genes, and unframed squares represent genes with only changes in position.\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/16d879bcf8fe3bee32524746.png"},{"id":49464629,"identity":"36a30392-58db-4249-9b5b-923f91b95bf4","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":1563934,"visible":true,"origin":"","legend":"\u003cp\u003eSynteny circular diagrams comparing the chloroplast genome of \u003cem\u003ePadina usoehtunii\u003c/em\u003e with species from six brown algal orders. Orange represents collinear regions, and gray represents inverted collinear regions.\u003c/p\u003e","description":"","filename":"Figure3.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/94e432cbd671d2dd19da1a53.png"},{"id":49464983,"identity":"5cf501dd-3ffa-44e0-8e9e-068fff87198c","added_by":"auto","created_at":"2024-01-11 09:27:29","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":126949,"visible":true,"origin":"","legend":"\u003cp\u003eBoxplots of dN/dS values of major functional group of genes in chloroplasts (a) and mitochondria (b) of 24 brown algae.\u003c/p\u003e","description":"","filename":"Figure4.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/57ba5446721971e750e7cc0d.png"},{"id":49464612,"identity":"6ade4443-aa21-450c-95df-93639bdeaed5","added_by":"auto","created_at":"2024-01-11 09:19:29","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":118627,"visible":true,"origin":"","legend":"\u003cp\u003eNon-synonymous (dN) and synonymous (dS) substitution rates for 115 chloroplast common PCGs (orange dots) and 35 mitochondrial common PCGs (blue dots) across 24 brown algae.\u003c/p\u003e","description":"","filename":"Figure5.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/9a7f5a237be2c400fa7dc64a.png"},{"id":49464616,"identity":"76484ec0-a446-41b8-808a-fcea40a0856c","added_by":"auto","created_at":"2024-01-11 09:19:29","extension":"png","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":158034,"visible":true,"origin":"","legend":"\u003cp\u003eNumbers of different repeated sequence types in organellar genomes of the Phaeophyceae species.\u003c/p\u003e","description":"","filename":"Figure6.png","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/e4d91fa71b5ff7b47259eeb8.png"},{"id":61793743,"identity":"2e9cdbd0-6b4e-4620-8438-5733026ec7e9","added_by":"auto","created_at":"2024-08-05 16:14:58","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":3859986,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/de3fa560-7f7c-4cc2-a184-01ecaa48df9e.pdf"},{"id":49464614,"identity":"eb48fe25-03ca-4aca-b2f1-e6b7ae11e0b1","added_by":"auto","created_at":"2024-01-11 09:19:29","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":360473,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS1.\u003c/strong\u003eGene circle map of the complete chloroplast genome of \u003cem\u003ePadina usoehtunii\u003c/em\u003e.\u003c/p\u003e","description":"","filename":"FigureS1.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/f77b403a2cdba97574e18346.pdf"},{"id":49464626,"identity":"17af2b9c-655f-4c63-9e8d-0e454f392188","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":290963,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS2.\u003c/strong\u003eGene circle map of the complete mitochondrial genome of \u003cem\u003ePadina usoehtunii\u003c/em\u003e.\u003c/p\u003e","description":"","filename":"FigureS2.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/038051ac03a892620c88c296.pdf"},{"id":49464988,"identity":"a4f152e1-bdf2-4902-a783-f5bdb0468056","added_by":"auto","created_at":"2024-01-11 09:27:30","extension":"pdf","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":350410,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS3.\u003c/strong\u003eSynteny circular diagrams comparing the chloroplast genome of \u003cem\u003ePadina usoehtunii\u003c/em\u003e with those of representatives of the Laminariales \u003cem\u003es.l.\u003c/em\u003e(p.1), Ectocarpales (p.2), and Fucales (p.3).\u003c/p\u003e","description":"","filename":"FigureS3.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/b876ae6af5e0feb1fcfaab28.pdf"},{"id":49464622,"identity":"644d4c7b-15ae-46c4-8f0c-cfc23fccc46b","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":1170756,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS4. \u003c/strong\u003eThe collinearity analysis of mitochondrial genomes of 12 brown algal species representing 6 orders.\u003c/p\u003e","description":"","filename":"FigureS4.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/88ff8f742c2500c5759d529e.pdf"},{"id":49464618,"identity":"1f1a8d62-31d1-4e6e-9b14-88dacf2bc9ce","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":677462,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS5.\u003c/strong\u003eThe collinearity analysis of chloroplast genomes of species from 5 brown algal orders. Yellow-marked areas indicate the short single copy (SSC) regions.\u003c/p\u003e","description":"","filename":"FigureS5.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/f871d34924886974210024a8.pdf"},{"id":49464630,"identity":"e8556afc-ba0f-4a3b-b71c-11220e40a1cd","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":6,"title":"","display":"","copyAsset":false,"role":"supplement","size":531647,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS6.\u003c/strong\u003eChloroplast (a) and mitochondrial (b) genes nonsynonymous to synonymous substitution ratios (dN/dS) among 24 selected Phaeophyceae species.\u003c/p\u003e","description":"","filename":"FigureS6.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/288d5a0ac7c2b78410ba5523.pdf"},{"id":49464623,"identity":"0c311356-9c79-40b8-9722-de9795b364dd","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":7,"title":"","display":"","copyAsset":false,"role":"supplement","size":1374683,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS7.\u003c/strong\u003e Relative synonymous codon usage (RSCU) in the chloroplast genomes of 6 orders in the Phaeophyceae.\u003c/p\u003e","description":"","filename":"FigureS7.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/afd7049f325610aca5f524e8.pdf"},{"id":49464991,"identity":"a5ce8c2f-2eeb-4cfe-9c1c-61bb1f98ccd6","added_by":"auto","created_at":"2024-01-11 09:27:30","extension":"pdf","order_by":8,"title":"","display":"","copyAsset":false,"role":"supplement","size":1555389,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS8.\u003c/strong\u003eRelative synonymous codon usage (RSCU) in the mitochondrial genomes of 6 orders in the Phaeophyceae.\u003c/p\u003e","description":"","filename":"FigureS8.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/f5f3a9de8d5e8bcb27aab81a.pdf"},{"id":49464627,"identity":"c31f46a0-df08-4b98-8c7e-6c823499522e","added_by":"auto","created_at":"2024-01-11 09:19:30","extension":"pdf","order_by":9,"title":"","display":"","copyAsset":false,"role":"supplement","size":946850,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFig\u003c/strong\u003e \u003cstrong\u003eS9.\u003c/strong\u003e Numbers of different short sequence repeat (SSR) types detected in chloroplast (a) and mitochondrial (b) genomes of 14 brown algae.\u003c/p\u003e","description":"","filename":"FigureS9.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/0d27cf946d86011a1749dd0d.pdf"},{"id":49464989,"identity":"4a8555b0-34a9-453b-ba65-bd4289b39f41","added_by":"auto","created_at":"2024-01-11 09:27:30","extension":"docx","order_by":10,"title":"","display":"","copyAsset":false,"role":"supplement","size":13573,"visible":true,"origin":"","legend":"","description":"","filename":"TableS1.docx","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/794ed8e08e30c95038ac1d74.docx"},{"id":49465692,"identity":"2b9a80e5-eee2-4822-b186-dc656f5df8b2","added_by":"auto","created_at":"2024-01-11 09:35:30","extension":"docx","order_by":11,"title":"","display":"","copyAsset":false,"role":"supplement","size":12619,"visible":true,"origin":"","legend":"","description":"","filename":"TableS2.docx","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/3535410dd0e9d400e1f19c15.docx"},{"id":49465693,"identity":"f3ef39be-4629-470a-aecf-267cdab92020","added_by":"auto","created_at":"2024-01-11 09:35:30","extension":"docx","order_by":12,"title":"","display":"","copyAsset":false,"role":"supplement","size":25941,"visible":true,"origin":"","legend":"","description":"","filename":"TableS3.docx","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/79f687ca55a72587216b12b4.docx"},{"id":49464986,"identity":"2b4dc7b8-947a-4c69-8793-5c79368ee095","added_by":"auto","created_at":"2024-01-11 09:27:30","extension":"docx","order_by":13,"title":"","display":"","copyAsset":false,"role":"supplement","size":13968,"visible":true,"origin":"","legend":"","description":"","filename":"TableS4.docx","url":"https://assets-eu.researchsquare.com/files/rs-3835960/v1/9c3a6984f34d40e461c879d2.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Comparative structure and evolution of the organellar genomes of Padina usoehtunii (Dictyotales) with the brown algal crown radiation clade","fulltext":[{"header":"Background","content":"\u003cp\u003eSemi-autonomous organelles in plant cells arose from ancient endosymbiotic events and subsequently underwent multiple gene transfers and structural modifications [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. Through this evolutionary process, organellar genomes have retained genes for essential organellar functions. Nowadays, with the increased availability of organellar genomes, it has become technically feasible to investigate genome-scale evolution, adaptation, and phylogenetic diversity across the algae tree of life.\u003c/p\u003e \u003cp\u003eThe brown algae or Phaeophyceae form a class of multicellular heterokont algae, currently classified into twenty orders and over 2,000 species [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. They often represent an essential component of the littoral and sublittoral zones in temperate and tropical ecosystems. This ancient and diverse lineage originated approximately 185\u0026thinsp;\u0026minus;\u0026thinsp;180\u0026nbsp;million years ago (Ma) [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. In brown algae, fossil evidence, including \u003cem\u003ePadina\u003c/em\u003e (Dictyotales; 145.5\u0026ndash;99.6 Ma) [\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e], \u003cem\u003ePaleocystophora\u003c/em\u003e (Fucales) and \u003cem\u003eJulescraneia grandicornis\u003c/em\u003e (Laminariales; 13\u0026ndash;17 Ma) [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e], along with the estimates of concatenated organellar genes [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e], suggest that the orders Dictyotales and Sphacelariales evolved earlier (\u0026gt;\u0026thinsp;100 Ma) than Desmarestiales/Laminariales/Ectocarpales (\u0026lt;\u0026thinsp;100 Ma) [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. The estimated brown algal divergence times reported that the order Dictyotales is a member of the SSDO clade (Sphacelariales, Syringodermatales, Dictyotales, and Onslowiales) or Dictyotophycidae that split from the BACR clade (brown algal crown radiation) or Fucophycidae and diversified into orders during the Jurassic (200\u0026thinsp;\u0026minus;\u0026thinsp;175 Ma) [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. Ectocarpales, Laminariales \u003cem\u003es.l.\u003c/em\u003e, Fucales, and Desmarestiales belonging to the BACR clade, diversified into orders during the early Cretaceous period (128 Ma). Taxonomically, the identification and classification of new brown algal species primarily relies on morphological characteristics and DNA sequences. Organellar genes in particular have shown better resolution for intraspecific discrimination in certain taxonomic groups compared to the nuclear internal transcribed spacer (ITS) [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. They have provided essential insights into the origin, phylogenetic structure and biogeographical patterns of brown algae [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e, \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. The application of organellar genomes has also been proved instrumental to uncover genetic relationships among individuals and populations, shedding light on adaptive evolution [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eMost phaeophycean organellar genomes sequenced to date are from members of the Fucophycidae (BACR clade) and only three species of Dictyotophycidae (SSDO clade), one Ishigeophycidae and no Discosporangiophycidae [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Notably, the structural and functional interpretation and comparison of the available organellar genomes seldom connected to the phylogenetic structure and timing of the brown algal tree of life. For example, a comparative study of mitochondrial and chloroplast genomes of \u003cem\u003eSargassum confusum\u003c/em\u003e (Fucales) found distinct evolutionary characteristics between the two organellar genomes in terms of A\u0026thinsp;+\u0026thinsp;T content, intron content, and stop codon usage, and reported that mitochondrial genomes exhibited more nucleotide variability than the chloroplast[\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. In addition, the estimated base substitution rates among seven \u003cem\u003eSargassum\u003c/em\u003e species in the Phaeophyceae showed higher mutation rates of mitochondrial genes compared to chloroplast genes [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e]. A more recent study of organellar genome rearrangements and evolution in nine orders of brown algae found that mitochondrial genes evolved at a faster rate than chloroplast genes, but that structural rearrangements in chloroplast genomes were more prevalent than in mitochondria [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. However, these studies either focused on a single genus or individual organellar genome, or biased taxa with data-rich organellar genomes. The limited number of organellar genomes from representatives outside the Fucophycidae may also lead to an incomplete or biased evolutionary interpretation of organellar genomes in the Phaeophyceae.\u003c/p\u003e \u003cp\u003eTo comprehensively elucidate the evolution and origin of brown algae, it is imperative to augment the organellar genome database from diverse brown algal taxa. The order Dictyotales represents a diverse and evolutionarily important lineage in the Phaeophyceae [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. Dictyotalean species are widely distributed in subtropical and tropical oceans and constitute one of the few brown algal taxa with high diversity in the tropics due to the tolerance to a warm climate [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. Among its diverse genera, the noteworthy genus \u003cem\u003ePadina\u003c/em\u003e Adanson encompasses 58 currently accepted and formally described species [\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e], but 63 operational taxonomic units (OTUs) [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. \u003cem\u003ePadina usoehtunii\u003c/em\u003e Ni-Ni-Win \u0026amp; H.Kawai is only known from the west coast of the Southeast Asian peninsula, from the Bay of Bengal (Myanmar) to the Malacca Strait (Thailand) where it grows in the intertidal [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e, \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e]. This species can potentially serve as a model for studying lineage diversity and genome evolution of brown algae.\u003c/p\u003e \u003cp\u003eIn this study, we sequenced the mitochondrial and chloroplast genomes of \u003cem\u003eP. usoehtunii\u003c/em\u003e, thereby adding to the organellar genome dataset of the order Dictyotales, which had previously consisted of two species (\u003cem\u003eDictyopteris divaricata\u003c/em\u003e (Okamura) Okamura and \u003cem\u003eDictyota dichotoma\u003c/em\u003e (Kuentze) O.Schmidt) within the family Dictyotaceae. Our study focused on the Dictyotales and compared it with five representative brown algal orders, i.e., Sphacelariales (Dictyotophycidae) and Desmarestiales, Laminariales \u003cem\u003es.l.\u003c/em\u003e, Ectocarpales, and Fucales (Fucophycidae). Mitochondrial genomes are available for two other orders (Ralfsiales, Ishigeales), but chloroplast genome are not available for these orders and therefore excluded from this study. Our investigation is centered on the following key aspects among brown algal organelles: 1) organellar genome features; 2) extent of structural rearrangements (inverted repeat regions and gene arrangements); 3) sequence evolutionary differences (nucleotide substitution rates, codon usage bias, and repeat sequences).\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eOrganellar genomes characteristics of \u003cem\u003ePadina usoehtunii\u003c/em\u003e\u003c/p\u003e \u003cp\u003eThe single-circular chloroplast genome of \u003cem\u003eP. usoehtunii\u003c/em\u003e is 125,291 bp in length (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e), larger than species of Fucales (124,068\u0026ndash;125,066 bp), but smaller than any other previously sequenced brown alga (126,099\u0026ndash;139,954 bp) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The largest phaeophycean chloroplast genome (139,954 bp) is found in \u003cem\u003eEctocarpus siliculosus\u003c/em\u003e (Dillwyn) Lyngbye (Ectocarpales). The chloroplast genome of \u003cem\u003eP. usoehtunii\u003c/em\u003e comprises a 72,226 bp Long Single Copy region (LSC), a 41,273 bp Short Single Copy region (SSC), and two 5,896 bp inverted repeats regions (IRa and IRb) (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). It contains 173 genes accounting for 78.02% of the chloroplast genome, including 139 protein coding genes (PCGs), 28 transfer RNA (tRNA) genes, and 6 ribosomal RNA (rRNA) genes (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). The \u003cem\u003erbc\u003c/em\u003eR and \u003cem\u003erpl\u003c/em\u003e32 genes were lost in both dictyotaleans, \u003cem\u003eP. usoehtunii\u003c/em\u003e and \u003cem\u003eDictyopteris divaricata\u003c/em\u003e, but present in all six other investigated orders. The \u003cem\u003ethiS\u003c/em\u003e gene was absent in the Dictyotales, Desmarestiales, and Ectocarpales, and three species of Laminariales \u003cem\u003es.l.\u003c/em\u003e (i.e., \u003cem\u003eChorda asiatica\u003c/em\u003e, \u003cem\u003eLaminaria ephemera\u003c/em\u003e, and \u003cem\u003eSaccharina japonica\u003c/em\u003e), but present in Fucales, Sphacelariales, and two species of Laminariales (i.e., \u003cem\u003eAlaria marginata\u003c/em\u003e and \u003cem\u003eMacrocystis pyrifera\u003c/em\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eGeneral features of organelle genomes in Phaeophyceae.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"15\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c12\" colnum=\"12\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c13\" colnum=\"13\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c14\" colnum=\"14\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c15\" colnum=\"15\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSpecies\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eOrder\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eFamily\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eGenBank\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"5\" nameend=\"c9\" namest=\"c5\"\u003e \u003cp\u003eMitochondrion\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c10\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eGenBank\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"5\" nameend=\"c15\" namest=\"c11\"\u003e \u003cp\u003eChloroplast\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eCDs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003etRNAs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003erRNAs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c8\"\u003e \u003cp\u003eORF\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c9\"\u003e \u003cp\u003eSize(bp)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c11\"\u003e \u003cp\u003eCDs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c12\"\u003e \u003cp\u003etRNAs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c13\"\u003e \u003cp\u003erRNAs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c14\"\u003e \u003cp\u003eORF\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c15\"\u003e \u003cp\u003eSize(bp)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ePadina usoehtunii\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDictyotales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eDictyotaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMW485979\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e36\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e32,303\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMW485982\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e125,291\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eDictyopteris divaricata\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDictyotales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eDictyotaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_043845\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e32,021\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_036804\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e27\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e126,099\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eDictyota dichotoma\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDictyotales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eDictyotaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_007685\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e31,617\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c14\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c15\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eProtohalopteris\u003c/em\u003e sp.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eSphacelariales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eStypocaulaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMZ156064\u003csup\u003ea)\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003en.d.\u003csup\u003ea)\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e41,306\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMZ156028\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e144\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e131,355\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eDesmarestia aculeata\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDesmarestiales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eDesmarestiaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMZ156052\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e40,822\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMZ156041\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e142\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e129,228\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eDesmarestia viridis\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDesmarestiales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eDesmarestiaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_007684\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e39,049\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c14\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c15\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum serratifolium\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_066463\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,793\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_066459\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,514\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum macrocarpum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_066462\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,766\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_066458\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,517\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum fulvellum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_066461\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,763\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_066457\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,277\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum confusum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_066460\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,719\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_066050\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,368\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum siliquastrum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_050651\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,765\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_064337\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e137\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,529\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum fusiforme\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMN883537\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,695\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMN794016\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,298\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum plagiophyllum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_064731\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,862\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_064732\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,536\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum polycystum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_064729\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e35\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,825\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_064730\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,493\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum hemiphyllum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_024861\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,686\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMT800998\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,319\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargassum horneri\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMH620963\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34,621\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_029856\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,068\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eCoccophora langsdorfii\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSargassaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_032287\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e35,660\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_032288\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e27\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,450\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSilvetia siliquosa\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eFucaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMW485976\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e36,036\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_061768\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e140\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e124,991\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eFucus spiralis\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFucales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eFucaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMG922856\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e36,396\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMG922855\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e125,066\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eChorda asiatica\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLaminariales \u003cem\u003es.l.\u003c/em\u003e\u003csup\u003eb)\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eChordaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMZ156050\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e41,788\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMZ156037\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e141\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e130,274\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAlaria marginata\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLaminariales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eAlariaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_058764\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e39,389\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_058769\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e141\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e130,582\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMacrocystis pyrifera\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLaminariales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eLaminariaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_065335\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e37,326\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_065334\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e141\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e130,201\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSaccharina japonica\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLaminariales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eLaminariaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eOP866273\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e37,657\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eOP866272\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e139\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e130,584\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eLaminaria ephemera\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLaminariales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eLaminariaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMZ156055\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e38\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e37,929\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMZ156035\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e142\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e130,610\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eEctocarpus siliculosus\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEctocarpales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eEctocarpaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMK045263\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e38,524\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_013498\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e148\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e139,954\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eEndarachne binghamiae\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEctocarpales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eScytosiphonaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_036747\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e37,460\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_038231\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e143\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e136,274\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eScytosiphon lomentaria\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEctocarpales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eScytosiphonaceae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNC_025240\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e36,918\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eNC_057081\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c11\"\u003e \u003cp\u003e137\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c12\"\u003e \u003cp\u003e27\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c13\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c14\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c15\"\u003e \u003cp\u003e134,485\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"15\"\u003e\u003csup\u003ea)\u003c/sup\u003e Mitochondrial genome annotation of \u003cem\u003eProtohalopteris\u003c/em\u003e sp. is incomplete.\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"15\"\u003e\u003csup\u003eb)\u003c/sup\u003e In this study, we adopted the old classification of Laminariales, \u003cem\u003eChorda asiatica\u003c/em\u003e belonged to Laminariales.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe single-circular mitochondrial genome (mitogenome) of \u003cem\u003eP. usoehtunii\u003c/em\u003e is composed 32,303 bp (Fig. \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e), similar to other Dictyotales species (31,617\u0026thinsp;\u0026minus;\u0026thinsp;32,021 bp, Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The mitogenome size in Dictyotales is smaller than in all other brown algal orders, including Ralfsiales and Ishigeales (REF) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The GC content of the exons and introns is, respectively, 35.40% and 40.24% (total GC content is 36.59%). The mitogenome has a high gene density (75.43%) and the conserved 36 PCGs, 25 tRNA genes, and 3 rRNA genes (Table \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e), are commonly found in the mitogenomes of brown algae. Most of the mitogenomes have a core set of 35 genes, i.e., \u003cem\u003eatp6\u003c/em\u003e, \u003cem\u003eatp8\u003c/em\u003e, \u003cem\u003eatp9\u003c/em\u003e, \u003cem\u003ecob\u003c/em\u003e, \u003cem\u003ecox1\u003c/em\u003e, \u003cem\u003ecox2\u003c/em\u003e, \u003cem\u003ecox3\u003c/em\u003e, \u003cem\u003enad1\u003c/em\u003e, \u003cem\u003enad2\u003c/em\u003e, \u003cem\u003enad3\u003c/em\u003e, \u003cem\u003enad4\u003c/em\u003e, \u003cem\u003ead4L\u003c/em\u003e, \u003cem\u003enad5\u003c/em\u003e, \u003cem\u003enad6\u003c/em\u003e, \u003cem\u003enad7\u003c/em\u003e, \u003cem\u003enad9\u003c/em\u003e, \u003cem\u003enad11\u003c/em\u003e, \u003cem\u003erpl2\u003c/em\u003e, \u003cem\u003erpl5\u003c/em\u003e, \u003cem\u003erpl6\u003c/em\u003e, \u003cem\u003erpl14\u003c/em\u003e, \u003cem\u003erpl16\u003c/em\u003e, \u003cem\u003erpl31\u003c/em\u003e, \u003cem\u003erps2\u003c/em\u003e, \u003cem\u003erps3\u003c/em\u003e, \u003cem\u003erps4\u003c/em\u003e, \u003cem\u003erps7\u003c/em\u003e, \u003cem\u003erps8\u003c/em\u003e, \u003cem\u003erps10\u003c/em\u003e, \u003cem\u003erps11\u003c/em\u003e, \u003cem\u003erps12\u003c/em\u003e, \u003cem\u003erps13\u003c/em\u003e, \u003cem\u003erps14\u003c/em\u003e, \u003cem\u003erps19\u003c/em\u003e and \u003cem\u003etatC\u003c/em\u003e. Only one Open Reading Frame (ORF) was found in \u003cem\u003eP. usoehtunii\u003c/em\u003e, located between \u003cem\u003eatp9\u003c/em\u003e and \u003cem\u003erpl16\u003c/em\u003e. It is also found in the other two Dictyotales, which both contain two more ORFs. In \u003cem\u003eP. usoehtunii\u003c/em\u003e only six genes (\u003cem\u003erpl2\u003c/em\u003e, \u003cem\u003erps19\u003c/em\u003e, \u003cem\u003erps3\u003c/em\u003e, \u003cem\u003erpl16\u003c/em\u003e, \u003cem\u003eORF121\u003c/em\u003e, and \u003cem\u003etatC\u003c/em\u003e) exist in the light strand with clockwise transcription direction (Fig. \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003ePhylogenetic assessment\u003c/p\u003e \u003cp\u003eMaximum Likelihood (ML) and Bayesian Inference (BI) trees were constructed using 115 and 35 common genes, respectively, from 27 chloroplast and 25 mitochondrial genomes (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The topologies of the ML and BI trees inferred from the chloroplasts and mitochondria genomes are highly congruent with maximum support values with the exception of the positions of the Desmarestiales and Fucales (Figs.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e and \u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The chloroplast gene based tree showed the Dictyotales to be the sister to all other sampled orders (Fucophycidae) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), because Sphacelariales (a member of the Dictyophycidae) was assigned to the outgroup. Desmarestiales is sister to a clade comprising the other three orders in the Fucophycidae. The phylogenetic relationships based on chloroplasts genes are consistent with the results published by [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. In contrast, in the mitochondrial gene-based tree, it is the Fucales that is sister to the other three fucophycidean orders (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Both organellar genomes demonstrated the monophyly of the Fucophycidae.\u003c/p\u003e \u003cp\u003eStructural variation in Phaeophyceae genomes\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eSynteny of organellar genome\u003c/h2\u003e \u003cp\u003eThe chloroplast co-linearity between \u003cem\u003ePadina usoehtunii\u003c/em\u003e (Dictyotales) and other brown algal species can help to better visualize their comparative genomic structures. The circular diagrams (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea) showed that the chloroplast genome of \u003cem\u003eP. usoehtunii\u003c/em\u003e is highly conserved in structure when compared to the closely related \u003cem\u003eDictyopteris divaricata\u003c/em\u003e (Dictyotaceae, Dictyotales). A total of 36 co-linear blocks spanning 75,525 bp were identified, and no inversions were observed (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea). In comparison to \u003cem\u003eProtohalopteris\u003c/em\u003e sp. (Sphacelariales), the co-linearity region covered 44,760 bp with 34 co-linear blocks and one identified inversion region (highlighted in gray, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eb) spanning 30,617 bp. The co-linearity between \u003cem\u003eP. usoehtunii\u003c/em\u003e and \u003cem\u003eDesmarestia aculeata\u003c/em\u003e (Desmarestiales) revealed 38 co-linear blocks covering 57,426 bp, which co-linear regions are smaller than that observed in \u003cem\u003eD. divaricata\u003c/em\u003e, but larger than that of \u003cem\u003eProtohalopteris\u003c/em\u003e sp. (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ec). Additionally, nine inversion regions (13,665 bp in total length) were identified in \u003cem\u003eDesmarestia aculeata\u003c/em\u003e. The co-linearity between \u003cem\u003eP. usoehtunii\u003c/em\u003e and five species within the order Fucales showed 29\u0026ndash;37 co-linear blocks, spanning 37,748 to 51,710 bp (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ed, Fig. \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e). Notably, the co-linear regions between \u003cem\u003eP. usoehtunii\u003c/em\u003e and most species within the order Fucales consisted predominantly of inversion regions, ranging from 24,932 to 38,959 bp. Among them, \u003cem\u003eSilvetia siliquosa\u003c/em\u003e (C.K.Tseng \u0026amp; C.F.Chang) E.A.Serr\u0026atilde;o, T.O.Cho, S.M.Boo \u0026amp; S.H.Brawley exhibited the highest proportion of inversion regions, accounting for 76% of the co-linear sequence. In comparison to five species within the order Laminariales, the co-linearity regions ranged from 47,115 to 52,827 bp, generally larger than those observed in Fucales (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ee, Fig. \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e). However, the frequency of gene inversions was much lower, with only 2\u0026ndash;5 inversion regions spanning 4,766 to 6,475 bp. When considering the co-linearity with Ectocarpales, \u003cem\u003eP. usoehtunii\u003c/em\u003e shared the smallest co-linear regions of 39,764 bp to 47,461 bp, 17 inversion blocks covering 24,446 bp to 28,947 bp (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ef, Fig. \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eRelative to the chloroplast genomes, the mitogenomes of brown algae are more conserved in structure (Fig. \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). Collinearity analysis of 12 brown algal mitogenomes showed that only Sphacelariales and Dictyotales underwent rearrangement, and other brown algae exhibited highly conserved mitogenomes. Mitogenome rearrangement of Dictyotales occurred in a small region, with \u003cem\u003eP. usoehtunii\u003c/em\u003e in the range of 10,400\u0026thinsp;\u0026minus;\u0026thinsp;10,950 bp and \u003cem\u003eDictyopteris divaricata\u003c/em\u003e in the range of 10,450\u0026thinsp;\u0026minus;\u0026thinsp;10,980 bp, and the reset gene is \u003cem\u003eatp9\u003c/em\u003e. \u003cem\u003eProtohalopteris\u003c/em\u003e sp. contained two rearrangement regions (excluding incomplete annotations), one at 2,000\u0026ndash;2,600 bp, with \u003cem\u003enad3\u003c/em\u003e and \u003cem\u003erps14\u003c/em\u003e in this region; the other at 14,000\u0026ndash;16,000 bp, with \u003cem\u003eatp9\u003c/em\u003e being identical to Dictyotales.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eGene distribution in IR boundary region\u003c/h2\u003e \u003cp\u003eAnalysis of the IR boundary regions of 25 brown algal chloroplast genes revealed a high degree of conservation in the IR region: \u003cem\u003erns\u003c/em\u003e, \u003cem\u003etrnI\u003c/em\u003e, \u003cem\u003etrnA\u003c/em\u003e, \u003cem\u003ernl\u003c/em\u003e, \u003cem\u003errn5\u003c/em\u003e, and \u003cem\u003erpl21\u003c/em\u003e (complete or partial). \u003cem\u003eEctocarpus siliculosus\u003c/em\u003e also includes \u003cem\u003etrnE\u003c/em\u003e, \u003cem\u003erpl32\u003c/em\u003e, \u003cem\u003etrnL\u003c/em\u003e, and \u003cem\u003epsbA\u003c/em\u003e in its IR region (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). However, the IR boundary regions exhibited different conservation levels. The boundary genes \u003cem\u003erns\u003c/em\u003e and \u003cem\u003eycf37\u003c/em\u003e of the IRa region and LSC region are the most conserved, except for the species of Ectocarpales. The boundary genes between LSC and IRb are \u003cem\u003ecbbx\u003c/em\u003e and \u003cem\u003erns\u003c/em\u003e in Sphacelariales, Desmarestiales, Fucales and Ectocarpales (except for \u003cem\u003eE. siliculosus\u003c/em\u003e), while \u003cem\u003etrnL\u003c/em\u003e and \u003cem\u003epsbY\u003c/em\u003e are found in species of Laminariales \u003cem\u003es.l.\u003c/em\u003e and Dictyotales (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The boundary genes \u003cem\u003ecbbx\u003c/em\u003e in the Sphacelariales, Desmarestiales, and Fucales is interchangeable in genomic position with \u003cem\u003etrnL\u003c/em\u003e in the Laminariales \u003cem\u003es.l.\u003c/em\u003e.\u003c/p\u003e \u003cp\u003eInversion of the SSC region was observed in different orders of the Phaeophyceae. The boundary and adjacent genes of the IRa and SSC regions are \u003cem\u003erpl21\u003c/em\u003e and \u003cem\u003erpl3\u003c/em\u003e (IRa-SSC direction) in the Dictyotales, Desmarestiales, Sphacelariales and Laminariales. The boundary and adjacent genes of IRb and SSC regions are \u003cem\u003erpl21\u003c/em\u003e (except for species of Laminariales which only have one \u003cem\u003erpl21\u003c/em\u003e in IRa-SSC) and \u003cem\u003eycf17\u003c/em\u003e/\u003cem\u003eycf19\u003c/em\u003e. Gene arrangement at the boundary of IRa-SSC and IRb-SSC regions is opposite to Ectocarpales and Fucales. Mauve collinearity analysis of chloroplast genomes of six brown algal orders showed that the entire SSC region of Dictyotales, Desmarestiales, Sphacelariales, and Laminariales species are inverted compared to those in Ectocarpales and Fucales (Fig. \u003cspan refid=\"MOESM5\" class=\"InternalRef\"\u003eS5\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eGene arrangement in mitogenome\u003c/h2\u003e \u003cp\u003eThe co-linearity analysis revealed the conserved nature of brown algal mitochondrial genome structures. The arrangement of core genes, including protein-coding genes (PCGs) and rRNA as well as tRNA genes, showed that the mitochondrial PCGs consisted of the same set of 35 genes across all investigated species, except \u003cem\u003eDesmarestia aculeata\u003c/em\u003e (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea). Only four genes (\u003cem\u003eatp8\u003c/em\u003e, \u003cem\u003eatp9\u003c/em\u003e, \u003cem\u003erps10\u003c/em\u003e, \u003cem\u003erpl31\u003c/em\u003e) that primarily encode components involved in ATP synthesis and ribosomal proteins exhibited variations in order across different species, with a reference to a representative species from the order Dictyotales. Additionally, \u003cem\u003eDesmarestia aculeata\u003c/em\u003e displayed an insertion of the \u003cem\u003erpo\u003c/em\u003e gene in the mitogenome. These findings indicate a high degree of conservation in the types and orders of PCGs in brown algal mitogenomes.\u003c/p\u003e \u003cp\u003eThe number of tRNA genes ranged from 23 to 26 among the brown algae (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eb). Most species possessed 25 tRNA genes, with the lowest number found in \u003cem\u003eE. siliculosus\u003c/em\u003e (Ectocarpales) and the highest in \u003cem\u003eSaccharina japonica\u003c/em\u003e (J.E.Areschoug) C.E.Lane, C.Mayes, Druehl \u0026amp; G.W.Saunders (Laminariales). Variations in tRNA gene arrangements were evident despite the relatively conserved numbers of tRNA genes. Using \u003cem\u003ePadina usoehtunii\u003c/em\u003e as a reference, the most common changes in tRNA gene positions occurred in \u003cem\u003etrnK\u003c/em\u003e (excluding \u003cem\u003eDictyota dichotoma\u003c/em\u003e), \u003cem\u003etrnE\u003c/em\u003e, \u003cem\u003etrnD\u003c/em\u003e and \u003cem\u003etrnA\u003c/em\u003e (excluding Dictyotales). In most cases, changes in the positions of \u003cem\u003etrnA\u003c/em\u003e and \u003cem\u003etrnD\u003c/em\u003e were linked. In Laminariales, the position of \u003cem\u003etrnA\u003c/em\u003e-\u003cem\u003etrnD\u003c/em\u003e occurred between \u003cem\u003etrnS1\u003c/em\u003e-\u003cem\u003etrnY2\u003c/em\u003e/\u003cem\u003etrnS2\u003c/em\u003e. The variability in the \u003cem\u003etrnE\u003c/em\u003e position was typically situated between \u003cem\u003etrnI\u003c/em\u003e and \u003cem\u003etrnK\u003c/em\u003e.\u003c/p\u003e \u003cp\u003eSequences variation in Phaeophyceae genomes\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eBase evolutionary rate\u003c/h2\u003e \u003cp\u003eNon-synonymous (dN) and synonymous (dS) substitution rates across 24 brown algal species encompassing five orders (Tables S3, S4) can help to understand sequence variations of chloroplast and mitochondrial common PCGs. Among the 115 chloroplast genes, the highest dN value was observed in \u003cem\u003erps20\u003c/em\u003e (0.3385), while the lowest values were found in \u003cem\u003epetN\u003c/em\u003e and \u003cem\u003epsbL\u003c/em\u003e (0.0001). The photosystem II genes \u003cem\u003epsbA\u003c/em\u003e, \u003cem\u003epsbE\u003c/em\u003e, and \u003cem\u003epsbK\u003c/em\u003e exhibited the lowest dS (0.3506\u0026ndash;0.3770) and relatively small dN values (0.0138\u0026ndash;0.0518). The dN/dS ratios were smallest for \u003cem\u003epetN\u003c/em\u003e (0.0001\u0026thinsp;\u0026lt;\u0026thinsp;\u0026lt;\u0026thinsp;1) and \u003cem\u003epsbL\u003c/em\u003e (0.0002\u0026thinsp;\u0026lt;\u0026thinsp;\u0026lt;\u0026thinsp;1) (Fig. \u003cspan refid=\"MOESM6\" class=\"InternalRef\"\u003eS6\u003c/span\u003ea), indicating an intense purifying selection. Conversely, the genes \u003cem\u003epetF\u003c/em\u003e and \u003cem\u003erpl9\u003c/em\u003e displayed the highest dN/dS ratios (0.4401\u0026thinsp;\u0026lt;\u0026thinsp;1, 0.3960\u0026thinsp;\u0026lt;\u0026thinsp;1), indicating a weak purifying selection.\u003c/p\u003e \u003cp\u003eThe dN/dS ratios for major functional gene categories, including ATP synthesis, photosystem, cytochrome b/f complex, chlorophyll biosynthesis and ribosomal proteins, revealed significant differences across these five functional groups (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ea). Specifically, ribosomal proteins exhibited significant differences in dN/dS ratios compared to genes involved in photosystem, light harvesting and chlorophyll biosynthesis (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.009). The highest average dN/dS ratio (0.1595) in ribosomal proteins indicates a much weak evolutionary pressure. The lowest average dN/dS ratios (0.0626, 0.0632) detected in genes involved in light harvesting, chlorophyll biosynthesis and photosystem categories suggest the strongest purifying selection.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eAmong the 35 mitochondrial genes, the highest dN/dS ratio occurred in ribosomal protein genes: \u003cem\u003erpl5\u003c/em\u003e (0.2825), \u003cem\u003erps10\u003c/em\u003e (0.2853), \u003cem\u003erps11\u003c/em\u003e (0.2952), \u003cem\u003erps2\u003c/em\u003e (0.3071), and \u003cem\u003erpl31\u003c/em\u003e (0.4309) (Fig. \u003cspan refid=\"MOESM6\" class=\"InternalRef\"\u003eS6\u003c/span\u003eb, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e), suggesting their relatively accelerated evolutionary rates. The lowest ratio was found in \u003cem\u003eatp9\u003c/em\u003e (0.0168). The dN/dS ratios for four functional groups in mitogenome (ATP synthase, cytochrome c oxidase, NADH dehydrogenase and ribosomal proteins) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eb), detected significantly high values in ribosomal protein genes compared to cytochrome c oxidase (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.009) and NADH dehydrogenase genes (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001).\u003c/p\u003e \u003cp\u003eSignificant differences in dN and dS values were observed between the mitochondrial genes and chloroplast genomes of brown algae (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001). The dN values of chloroplast genes ranged from 0.0001 to 0.3385, whereas those of mitochondria ranged from 0.0062 to 0.4213 (Tables S3-S4). The dS values of chloroplast genes ranged from 0.3506 to 1.1051, whereas the mitochondrial ones ranged from 0.9423 to 2.0364 (except \u003cem\u003eatp9\u003c/em\u003e, dS\u0026thinsp;=\u0026thinsp;0.3697). Most mitochondrial genes generally showed higher dS and dN values than the chloroplast genes (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e), indicating that mitochondrial genes had higher mutation rates than the chloroplast genes in brown algae. The dN/dS values of chloroplast genes ranged from 0.0098 to 0.4401 (except \u003cem\u003epetN\u003c/em\u003e (dN/dS\u0026thinsp;=\u0026thinsp;0.0001) and \u003cem\u003epsbL\u003c/em\u003e (dN/dS\u0026thinsp;=\u0026thinsp;0.0002)) and those of mitochondrial genes ranged from 0.0168 to 0.4309 (Fig. \u003cspan refid=\"MOESM6\" class=\"InternalRef\"\u003eS6\u003c/span\u003e). This statistically non-significant difference (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.724) manifests that they both experienced purifying selection at similar levels.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eCodon usage\u003c/h2\u003e \u003cp\u003eRSCU values revealed the use preferences of 61 codons (excluding three stop codons) in brown algae. AUU was the most frequent codon for Leu in chloroplast and mitochondrial genomes. Approximately 25\u0026ndash;27 codons (RSCU\u0026thinsp;\u0026gt;\u0026thinsp;1) were preferred in organellar genomes. RSCU\u0026thinsp;\u0026gt;\u0026thinsp;1.6 is considered as over-preference for codons, while RSCU\u0026thinsp;\u0026lt;\u0026thinsp;0.6 expresses that codons are under-preferred [\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e]. Accordingly, 13 codons were identified as frequently used codons (RSCU\u0026thinsp;\u0026gt;\u0026thinsp;1.6, average RSCU\u0026thinsp;=\u0026thinsp;2.00) whereas 27 codons were underused (RSCU\u0026thinsp;\u0026lt;\u0026thinsp;0.6, average RSCU\u0026thinsp;=\u0026thinsp;0.28) in chloroplast genomes (Fig. \u003cspan refid=\"MOESM7\" class=\"InternalRef\"\u003eS7\u003c/span\u003e). In mitogenomes, there were four over-preferred codons (RSCU\u0026thinsp;\u0026gt;\u0026thinsp;1.6, average RSCU\u0026thinsp;=\u0026thinsp;2.26) and eight under-preferred codons (RSCU\u0026thinsp;\u0026lt;\u0026thinsp;0.6, average RSCU\u0026thinsp;=\u0026thinsp;0.30) (Fig. \u003cspan refid=\"MOESM8\" class=\"InternalRef\"\u003eS8\u003c/span\u003e). The codon bias of the chloroplast genome is stronger than that of the mitogenome in brown algae and the third position of frequently used codons was predominantly A or U.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eRepeat sequences\u003c/h2\u003e \u003cp\u003eA total of 105 (\u003cem\u003ePadina usoehtunii\u003c/em\u003e) to 157 (\u003cem\u003eChorda asiatica\u003c/em\u003e Sasaki \u0026amp; Kawai) simple sequence repeats (SSRs) were detected in 14 chloroplast genomes, including 81\u0026ndash;113 mononucleotides (mono-), 4\u0026ndash;16 dinucleotides (di-), 3\u0026ndash;13 trinucleotides (tri-), 4\u0026ndash;15 tetranucleotides (tetra-), 0\u0026ndash;5 pentanucleotide (penta-), and 0\u0026ndash;2 hexanucleotide (hexa-) (Fig. \u003cspan refid=\"MOESM9\" class=\"InternalRef\"\u003eS9\u003c/span\u003e). In 14 mitogenomes analyzed, there are 22 (\u003cem\u003eP. usoehtunii\u003c/em\u003e) to 52 (\u003cem\u003eE. siliculosus\u003c/em\u003e and \u003cem\u003eScytosiphon lomentaria\u003c/em\u003e (Lyngbye) Link) SSRs, and the numbers of mono-, di-, tri-, tetra-, penta-, and hexa-nucleotide are 20\u0026ndash;47, 0\u0026ndash;3, 0\u0026ndash;2, 0\u0026ndash;4, 0\u0026ndash;1, 0\u0026ndash;1, respectively (Fig. \u003cspan refid=\"MOESM9\" class=\"InternalRef\"\u003eS9\u003c/span\u003e). The most numerous mononucleotides repeats are of the A and T type. \u003cem\u003eP. usoehtunii\u003c/em\u003e had the least numbers of SSRs among brown algae. We identified the forward (F), reverse (R), palindromic (P), and complementary (C) repeat sequences in chloroplast and mitochondrial genomes of brown algae (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e). Palindromic repeats are the most frequent in chloroplast genomes, while forward repeats are the most frequent type in mitogenomes. Complementary repeats are the least frequent type in both organelle genomes. The amount of these long repeat sequences was highly variable in mitogenomes, with 38 forward repeats and 6 palindromic repeats in \u003cem\u003eProtohalopteris\u003c/em\u003e sp., 20 forward repeats and 15 palindromic repeats in \u003cem\u003eP. usoehtunii\u003c/em\u003e. In chloroplast genomes, the numbers of different repeat types is more conservative within the same brown algal order.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eWhen codon bias, number and types of repeat sequences, and particularly genome size and structure, were mapped on the phylogenetic tree of the Phaeophyceae, varying degrees of diversity at the order level became apparent (Figs.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e and \u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The structural differences in chloroplast genome primarily reflected on the size and types of genes at the IR boundary region and the rearrangement of the SSC region, which may mechanically be related to gene replication. In brown algae, chloroplast genomes are more variable in structure, while mitochondrial genomes exhibit higher sequence variation. This pattern is similar in red algae [\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e, \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e], but contrasts that in land plants and green algae [\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e]. The rate of sequence evolution is likely influenced by the extent of organellar genome modification as observed in terrestrial plants [\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eOrganelle genome size and gene loss\u003c/p\u003e \u003cp\u003eThe Dictyotales with divergence time around 155 Ma [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e] has a smaller chloroplast genome size, compared to later divergence clades within the BACR clade, except Fucales (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), which has a similar chloroplast genome size as Dictyotales (around 125 kb). Previous researches showed a positive correlation between chloroplast genome size and the total length of non-coding sequences [\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e], suggesting that the accumulation of non-coding regions contributes to larger chloroplast genomes, possibly facilitating the emergence of new genes.\u003c/p\u003e \u003cp\u003eIn comparison with other orders of Phaeophyceae, Dictyotales exhibits distinctive gene losses in its chloroplast genome: \u003cem\u003erbcR\u003c/em\u003e and \u003cem\u003erpl32\u003c/em\u003e (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). \u003cem\u003eRbcR\u003c/em\u003e is a potential transcriptional regulator of Rubisco and its absence has not been observed in other brown algal lineages. Horizontal gene transfer likely occurred between the organelles and the nucleus in Dictyotales, leading to the presence of \u003cem\u003erbcR\u003c/em\u003e in the nucleus [\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e]. This hypothesis requires further validation. \u003cem\u003eRpl32\u003c/em\u003e has been found to be lost in 21 algal chloroplast genomes, mostly belonging to the Streptophyta, like some seed plants: eudicots, gymnosperms, magnoliids, and monocots [\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e]. Gene loss events within chloroplast genomes have been observed in other Ochrophyta lineages such as Dictyochophyceae and Synurophyceae [\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e, \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e], suggesting that these gene loss events are not uncommon during the course of evolution. The loss of \u003cem\u003erbcR\u003c/em\u003e and \u003cem\u003erpl32\u003c/em\u003e genes happened after the SSDO-BACR split, because secondary gain of these genes in the BACR clade is highly unlikely. We do not know whether these genes were lost early during SSDO evolution or whether it happened later, because no SSDO chloroplasts other than those from the Dictyotales have been sequenced.\u003c/p\u003e \u003cp\u003eVariation of organelle genome structure\u003c/p\u003e \u003cp\u003eStructural comparison of chloroplast genomes between \u003cem\u003ePadina usoehtunii\u003c/em\u003e and other orders revealed clear differences across the phylogenetic tree of brown algae. The BACR orders Laminariales, Fucales, and Desmarestiales showed large structural differences compared to Dictyotales in chloroplast genome organization (Fig. \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e). Notably, Dictyotales displayed a smaller number of inverted regions compared to the Laminariales than to the Fucales and Ectocarpales (Fig. \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e). A certain degree of chloroplast genome structural instability can generate adaptive and recovery mechanisms to cope with environmental changes, accelerating the evolutionary trajectory of brown algae and aiding their expansion into a wide range of geographical environments [\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThe IR region is crucial in terrestrial plants as it stabilizes chloroplast genome organization, mediates intramolecular recombination, and increases the copy number of rRNA genes [\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e]. The expansion and contraction of the IR region are linked to the addition or reduction of boundary genes (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The size of the IR region varies significantly among different Ochrophyta algae, such as Raphidophyceae and Bacillariophyceae, which have IR sizes of 18\u0026ndash;22 kb, approximately three times larger than that in brown algae (5\u0026ndash;9 kb). The IR region in brown algae includes rRNA and tRNA genes, while in the Raphidophyceae and Bacillariophyceae it also contains ribosomal protein genes such as \u003cem\u003erpl32\u003c/em\u003e, \u003cem\u003erpl21\u003c/em\u003e, \u003cem\u003erpl34\u003c/em\u003e, as well as photosystem II genes \u003cem\u003epsbA\u003c/em\u003e, \u003cem\u003epsbY\u003c/em\u003e, and \u003cem\u003epsbC\u003c/em\u003e [\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e]. The IR region structure in oogamous (with maternal chloroplast inheritance) Dictyotales, Laminariales, and Fucales, is relatively conserved, while substantial structural variation is observed among different species of isogamous Ectocarpales (with biparental chloroplast inheritance), which accumulate more variation compared to oogamous brown algae, leading to a higher rate of structural rearrangements [\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e].\u003c/p\u003e \u003cp\u003e \u003cem\u003eRpl21\u003c/em\u003e is a common gene between the IR and SSC boundary regions in brown algae. The contraction or expansion of the IR region can affect the location of \u003cem\u003erpl21\u003c/em\u003e (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). When the IR region is large, the \u003cem\u003erpl21\u003c/em\u003e gene and its replicates are present in the IRa and IRb, as in the Dictyotales (IR: 5.8-6 kb), Sphacelariales (IR: 5.9 kb), and Ectocarpales (IR: 5.5\u0026ndash;8.6 kb). When the IR region is small, \u003cem\u003erpl21\u003c/em\u003e will span the IR and SSC regions, as in the Desmarestiales (IR: 5.3 kb), Fucales (IR: 3.4\u0026ndash;5.4 kb), and Laminariales (IR: 5.4\u0026ndash;5.5 kb). The inversion of the entire SSC region happened two times, the first occurred between 144.6\u0026ndash;54.6 Ma, after the split of the Fucales from the Desmarestiales, and the second occurred between 125.0-51.5 Ma, after the split of the Ectocarpales from the Laminariales \u003cem\u003es.l.\u003c/em\u003e. (Fig. \u003cspan refid=\"MOESM5\" class=\"InternalRef\"\u003eS5\u003c/span\u003e) [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. This extensive inversion might have arisen due to the replication mechanisms, such as recombination-dependent replication (RDR). During replication, invasions mediated by reverse repeats in the plastid genome result in gene conversion carried out through unidirectional crossovers, thereby giving rise to single-copy region inversions [\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e].\u003c/p\u003e \u003cp\u003ePhylogenetic analysis showed that the \u003cem\u003ecbbx\u003c/em\u003e gene originated in cyanobacteria [\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e]. The CbbX protein can function as an activase of inhibited red-type Rubisco [\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e]. \u003cem\u003ecbbx\u003c/em\u003e in the brown alga \u003cem\u003eSaccharina japonica\u003c/em\u003e has been reported to exist in the nuclear and in the chloroplast genome [\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e]. The nuclear-encoded \u003cem\u003ecbbx\u003c/em\u003e (\u003cem\u003ecbbx-n\u003c/em\u003e) exhibits higher enzyme activity compared to the plastid-encoded \u003cem\u003ecbbx\u003c/em\u003e (\u003cem\u003ecbbx-p\u003c/em\u003e). \u003cem\u003eCbbx-n\u003c/em\u003e can interact with \u003cem\u003ecbbx-p\u003c/em\u003e to form a heterohexamer, promoting higher catalytic efficiency of Rubisco, thereby accelerating the rate of carbon assimilation in photosynthesis. The rearrangements of the \u003cem\u003ecbbx\u003c/em\u003e gene in certain brown algal lineages may affect the catalyzing efficiency of Rubisco, thus influencing the rate of carbon assimilation in photosynthesis. However, this hypothesis requires further experimental validation.\u003c/p\u003e \u003cp\u003eVariation of organellar genome sequence\u003c/p\u003e \u003cp\u003eWe found a significantly higher non-synonymous (dN) substitution rate in mitochondrial genes compared to chloroplast genes, which is consistent with the previous research on the evolutionary rate in brown algae [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. The average synonymous (dS) substitution rate in mitochondria is higher than in chloroplasts, although this distinction is not clearly discernible in the scatterplot in Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e. This observation may be attributed to the inclusion of Dictyotales and Sphacelariales. Nevertheless, when considering the entire organellar genome dataset, it is evident that brown algal mitochondrial genes have a faster mutation rate than chloroplasts genes (Table \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e-\u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). This was also observed in the phytoplankton \u003cem\u003ePhaeocystis\u003c/em\u003e (Haptophyta) and the red alga \u003cem\u003ePorphyra\u003c/em\u003e [\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e, \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e], but this trend was in contrast to most land plants, where the dS value of mitochondria were three times lower than the chloroplasts [\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eFor both chloroplast and mitochondrial genomes, the average dN/dS values for all protein coding genes (PCGs) are less than 1, suggesting that these genes have undergone purifying selection. However, genes from different functional categories showed variable dN/dS values. Notably, the ribosomal protein genes, whether in chloroplasts or in mitochondria, exhibited the highest average dN/dS values, suggesting a much weaker purifying selection on it. In the chloroplast genomes, the strongest purifying selection is observed in the photosystem genes, consistent with the predicted dN/dS values for the primary functional groups of 23 brown algal species reported recently [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. These differences of the dN/dS values with different function genes reflected variation in the strength of purifying selection.\u003c/p\u003e \u003cp\u003eHighly preferred codons in both chloroplast and mitochondrial genomes all ended with A/U, while less preferred codons ended with C/G (Figs. S7-S8). Codon preference analysis indicates that codon usage patterns are similar among different brown algal species. However, codon bias in the brown algal chloroplast genome is higher than in the mitochondrial genome. Selective pressure and gene mutations are likely important factors to influence codon usage [\u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e], possibly due to the high AT content in organellar genomes which can potentially lead to a bias towards AU in codons. Next, sequencing more organellar genome of representative taxon can largely contribute to the understanding of the structural genomics and molecular evolution of the brown algal tree of life.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cp\u003eSample collection and DNA extraction\u003c/p\u003e \u003cp\u003e \u003cem\u003ePadina usoehtunii\u003c/em\u003e was collected from the intertidal at Pakarang Cape (8\u0026ordm;44'17.9\"N 98\u0026ordm;13'05.5\"E) in Phang-nga province on the Andaman coast of Thailand in December 2019, silica-dried and transported to Qingdao, China. Species identification was \u003cem\u003ea posteriori\u003c/em\u003e confirmed by comparing mitocondrial \u003cem\u003ecox\u003c/em\u003e1 and chloroplast-encoded \u003cem\u003erbc\u003c/em\u003eL gene sequences to the representative DNA sequences of the \u003cem\u003eP. usoehtunii\u003c/em\u003e type specimen (Genbank AB512597 and AB512559, respectively). The total DNA was extracted from young thallus using the FastPure\u0026reg; Plant DNA Isolation Mini Kit (Vazyme Biotech Co., China). The extracted DNA was purified using a DNA Purification Kit (Vazyme Biotech Co., China) according to manufacturer\u0026rsquo;s instructions.\u003c/p\u003e \u003cp\u003eGenome sequencing, assembly and annotation\u003c/p\u003e \u003cp\u003eTo obtain full-length chloroplast and mitochondria genome sequences, we used the paired-end (Illumina Hiseq) strategy in this study. First, approximately 1 \u0026micro;g of purified DNA was made into libraries using the TruSeq\u0026trade; Nano DNA Sample Prep Kit from Illumina according to the manufacturer\u0026rsquo;s protocol. Libraries were sequenced using an Illumina Hiseq 4000 with 150 bp paired-end reads length (Biozeron, Shanghai, China). The raw reads were checked with FastQC and trimmed by Trimmomatic-0.39 [\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e]. Algal organellar genomes assembly was performed using NOVOPlasty v2.7.2 software (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://github.com/ndierckx/NOVOPlasty\u003c/span\u003e\u003cspan address=\"https://github.com/ndierckx/NOVOPlasty\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e). The near-source reference genome was used as the seed sequence, with the remaining parameters set as default. Clean reads were compared back on the Scaffold obtained by assembly, and based on the paired-end and overlap of reads, the assembly results were partially assembled and optimized. GapCloser v1.12 (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://soap.genomics.org.cn/soapdenovo.html\u003c/span\u003e\u003cspan address=\"http://soap.genomics.org.cn/soapdenovo.html\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) was used to repair the internal holes in the assembly.\u003c/p\u003e \u003cp\u003eThe mitochondrial and chloroplast genes were annotated using the online GeSeq tool (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://chlorobox.mpimp-golm.mpg.de/geseq.html/\u003c/span\u003e\u003cspan address=\"https://chlorobox.mpimp-golm.mpg.de/geseq.html/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) to predict protein coding genes, tRNA and rRNA, using following parameters: Protein search identity: 60; rRNA, tRNA, DNA search identity: 35; 3rd Party tRNA annotators: tRNAscan-SE. The position of each coding gene was determined using BLAST [\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e] searches against reference genes. Manual corrections of genes for start/stop codons and for intron/exon boundaries were performed in SnapGene Viewer. The circular maps of genomes were displayed using the software OGDRAW (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://chlorobox.mpimp-golm.mpg.de/OGDraw.html\u003c/span\u003e\u003cspan address=\"https://chlorobox.mpimp-golm.mpg.de/OGDraw.html\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e). Gene function annotation was performed with available protein databases by BLASTp (evalue\u0026thinsp;\u0026le;\u0026thinsp;10\u003csup\u003e\u0026minus;\u0026thinsp;5\u003c/sup\u003e), including NCBI Non-Redundant Protein Sequence Database (NR), Swiss-Prot, Clusters of Orthologous Groups (COGs), and Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) terms. Finally, we submitted the mitochondrial and chloroplast genomes of \u003cem\u003ePadina usoehtunii\u003c/em\u003e to the GenBank database with accession numbers MW485979 and MW485982, respectively.\u003c/p\u003e \u003cp\u003ePhylogenetic analysis\u003c/p\u003e \u003cp\u003eWe selected 27 and 25 species from 6 orders of Phaeophyceae (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) to construct mitochondrial and chloroplast phylogenetic trees respectively, using \u003cem\u003eProtohalopteris\u003c/em\u003e sp. (Sphacelariales) as outgroup. Sequences of 35 and 115 shared genes from mitogenomes and chloroplast genomes were aligned by mafft v7.313 [\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e] and the sequences were corrected with Gblock 0.91b [\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e]. IQtree v.1.6.8 [\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e, \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e, \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e] and MrBayes 3.2.6 [\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e] were used to construct Maximum likelihood (ML) and Bayesian inference (BI) trees, respectively. ModelFinder [\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e] was used to select the best nucleotide substitution model based on Akaike information criterion (AIC). The best-fit models GTR\u0026thinsp;+\u0026thinsp;F\u0026thinsp;+\u0026thinsp;I\u0026thinsp;+\u0026thinsp;G4 (G\u0026thinsp;=\u0026thinsp;0.232, I\u0026thinsp;=\u0026thinsp;0.800) and GTR\u0026thinsp;+\u0026thinsp;F\u0026thinsp;+\u0026thinsp;I\u0026thinsp;+\u0026thinsp;G4 (G\u0026thinsp;=\u0026thinsp;0.352, I\u0026thinsp;=\u0026thinsp;0.853) were used for mitochondria and chloroplast, respectively. For ML tree construction, the parameters were set to 1000 ultrafast bootstrap replicates with others as default [\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e]. For BI tree, the Markov Chain Monte Carlo (MCMC) were set to 1\u0026times;10\u003csup\u003e6\u003c/sup\u003e generations running with a tree sampling frequency of every 1000 generations and the first 25% was discarded as burn-in. Finally, FigTree v1.4.4 (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://tree.bio.ed.ac.uk/software/figtree/\u003c/span\u003e\u003cspan address=\"http://tree.bio.ed.ac.uk/software/figtree/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) was used to beautify the tree files.\u003c/p\u003e \u003cp\u003eGenome synteny and IR boundary regions analysis\u003c/p\u003e \u003cp\u003eWe used TBtools v1.108 to map the collinearity of chloroplast genome structure between \u003cem\u003eP. usoehtunii\u003c/em\u003e and six species from the Dictyotales, Sphacelariales, Desmarestiales, Laminariales, Ectocarpales, and Fucales, respectively [\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e]. The species annotation order was manually adjusted to be consistent to ensure correct collinear correspondence. BLAST [\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e] was used to match synteny, sequences with less than 100 bp were removed, and only a pair of IR collinear information (IRa-IRa, IRb-IRb) was retained. Mauve [\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e] was used to detect linear collinearity of chloroplast genomes, setting to align with progressive Mauve. In order to explore the differences of chloroplast LSC/IR/SSC region boundaries, we plotted the genes between each partition by CPJSdraw v1.0.0 [\u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e58\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eBase substitution rate estimation\u003c/p\u003e \u003cp\u003eTo explore evolutionary rates of brown algal organelle genomes, we extracted 35 and 115 shared PCGs from 24 species whose both organelles have been sequenced using PhyloSuite v1.2.2 [\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e]. The genome datasets of Phaeophyceae were obtained from GenBank (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). MAFFT [\u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e] and Gblocks [\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e] were used for sequence alignment and correction, respectively. The aligned sequence was converted into pml format by PhyloSuite v1.2.2 [\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e]. We used PAML v4.10 [\u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e62\u003c/span\u003e] to estimate non-synonymous (dN) and synonymous substitution (dS) of 24 mitogenomes and chloroplast genomes. The parameters set to runmode\u0026thinsp;=\u0026thinsp;0 and CodonFreq\u0026thinsp;=\u0026thinsp;2. To avoid data bias we calculated the median pairwise comparisons data of each gene. The histogram was drawn to show dN/dS values of each gene. The scatter plot was drawn to show the tendency of differences in dN/dS values among chloroplasts and mitochondria. We used the Kruskal-Wallis test in SPSS v26.0 software (IBM, Armonk, NY, USA) to explore the diversity in dN/dS values of different functional genes. The comparison of substitution rate between the two organelles was also tested using the method above.\u003c/p\u003e \u003cp\u003eRepeat sequences and codon preference analysis\u003c/p\u003e \u003cp\u003eShort Sequence Repeats (SSRs) were identified using MISA [\u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e63\u003c/span\u003e]. The parameter settings were as follows: mono-, di-, tri-, tetra-, pent-, and hexa-nucleotide motifs have at least 8, 5, 4, 3, 3 and 3 repeats, respectively. We used REPuter (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://bibiserv.techfak.uni-bielefeld.de/reputer\u003c/span\u003e\u003cspan address=\"http://bibiserv.techfak.uni-bielefeld.de/reputer\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) to detect forward (F), palindromic (P), reverse (R) and complementary (C) repeats with Hamming distance equal to 3 and minimum repeat size of 20 bp [\u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e64\u003c/span\u003e]. The PCGs of organelles were extracted by PhyloSuitev1.2.2 [\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e]. CodonW1.4.4 [\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e] was used to calculate the relative synonymous codon usage (RSCU) of each PCGs. RSCU\u0026thinsp;=\u0026thinsp;1 means no bias in codon usage. RSCU\u0026thinsp;\u0026lt;\u0026thinsp;1 indicates less codon usage, while RSCU\u0026thinsp;\u0026gt;\u0026thinsp;1 shows more preference in codon usage [\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e].\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eAIC: Akaike information criterion; BACR: Brown algal crown radiation; BI: Bayesian inference; \u003cem\u003eCbbx\u003c/em\u003e-n: Nuclear-encoded cbbx; \u003cem\u003eCbbx\u003c/em\u003e-p: Plastid-encoded cbbx; COGs: Clusters of Orthologous Groups; dN: Non-synonymous substitution; dS: Synonymous substitution; GO: Gene Ontology; IR: Inverted repeat; ITS: Internal transcribed spacer; KEGG: Kyoto Encyclopedia of Genes and Genomes; LSC: Long single copy; Ma: Mega-annum; MCMC: Markov Chain Monte Carlo; ML: Maximum likelihood; NR: Non-Redundant Protein Sequence Database; ORF: Open Reading Frame; PCGs: Protein coding genes; RDR: Recombination-dependent replication; rRNAs: Ribosomal RNA genes; SSC: Short single copy; SSDO: Sphacelariales, Syringodermatales, Dictyotales, and Onslowiales; tRNAs: Transfer RNA genes;\u003c/p\u003e"},{"header":"Declarations","content":" \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eData Availability\u003c/h2\u003e \u003cp\u003eThe datasets used in this study are entirely included in the article and supplementary files. Availability and usage of the datasets require the consent of the corresponding author. The GenBank accession numbers of the chloroplast and mitochondrial genomes of \u003cem\u003ePadina usoehtunii\u003c/em\u003e are MW485982 and MW485979, respectively. The chloroplast and mitochondrial genomes data of other brown alga were obtained from NCBI.\u003c/p\u003e \u003c/div\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe are grateful for the joint support from the National Natural Science Foundation of China (32371697), the National Natural Science Foundation of China (41761144057) and the Thailand Research Fund (RDG6130002).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors\u0026rsquo; contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eZi-Min Hu and Stefano G. A. Draisma led this project. Yi-Jia Liu, Tong-Yun Zhang and Qi-Qi Wang collectively conducted the experiments and performed data analysis. Yi-Jia Liu drafted the manuscript. Zi-Min Hu provides important advice on writting. Stefano G. A. Draisma collected the samples and revised the manuscript. All authors approved the final version of the manuscript for publication.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by National Natural Science Foundation of China (32371697), a joint research grant between National Natural Science Foundation of China (41761144057) and Thailand Research Fund (RDG6130002).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eSample collection permission\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe field collection of seaweed samples in this article complies with the relevant Thailand and international guidelines/regulations/ legislation.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor details\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003csup\u003e1\u003c/sup\u003eOcean School, Yantai University, Yantai 264005, China. \u003csup\u003e2\u003c/sup\u003eExcellence Center for Biodiversity of Peninsular Thailand, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90110, Thailand.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eKurland CG, Andersson SG. Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev. 2000;64(4):786\u0026ndash;820.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKutschera U, Niklas KJ. Endosymbiosis, cell evolution, and speciation. Theory Biosci. 2005;124(1):1\u0026ndash;24.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBrindefalk B, Ettema TJ, Viklund J, Thollesson M, Andersson SG. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS ONE. 2011;6(9):e24457.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCock JM, Sterck L, Rouz\u0026eacute; P, Scornet D, Allen AE, Amoutzias G, et al. The \u003cem\u003eEctocarpus\u003c/em\u003e genome and the independent evolution of multicellularity in brown algae. Nature. 2010;465:617\u0026ndash;21.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSilberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the brown algal crown radiation. Mol Phylogenet Evol. 2010;56(2):659\u0026ndash;74.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRajanikanth A. A fossil marine brown alga from the Gangapur Formation, Pranhita-Godavari Graben. Curr Sci. 1989;58(2):78\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eParker BC, Dawson EY. Non-calcareous marine algae from California Miocene deposits. Nova Hedwigia Beihefte. 1965;10:273\u0026ndash;95.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eReviers BD, Rousseau F. Towards a new classification of the brown algae. Phycol Res. 1999;13(1):107\u0026ndash;201.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDraisma SGA, van Prud'homme WF, Stam WT, Olsen JL. A reassessment of phylogenetic relationships within the Phaeophyceae based on Rubisco large subunit and ribosomal DNA sequences. J Phycol. 2001;37(4):586\u0026ndash;603.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBringloe TT, Starko S, Wade RM, Vieira C, Kawai H, Clerck OD, et al. Phylogeny and evolution of the brown algae. Crit Rev Plant Sci. 2020;39(4):281\u0026ndash;321.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWei L, Xin Y, Wang D, Jing X, Zhou Q, Su X, et al. \u003cem\u003eNannochloropsis\u003c/em\u003e plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. BMC Genomics. 2013;14:534.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMuhlin JF, Brawley SH. Recent versus relic: discerning the genetic signature of \u003cem\u003eFucus vesiculosus\u003c/em\u003e (Heterokontophyta; Phaeophyceae) in the Northwestern Atlantic. J Phycol. 2009;45(4):828\u0026ndash;37.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHu ZM, Uwai S, Yu SH, Komatsu T, Duan DL. Phylogeographic heterogeneity of the brown macroalga \u003cem\u003eSargassum horneri\u003c/em\u003e (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol. 2011;20(18):3894\u0026ndash;909.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHu ZM, Kantachumpoo A, Liu RY, Sun ZM, Yao JT, Komatsu T, Uwai S, Duan DL. A late Pleistocene marine glacial refugium in the south-west of Hainan Island, China: phylogeographical insights from the brown alga \u003cem\u003eSargassum polycystum\u003c/em\u003e. J Biogeogr. 2018;45:355\u0026ndash;66.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLi JJ, Hu ZM, Sun ZM, Yao JT, Liu FL, Fresia P, Duan DL. Historical isolation and contemporary gene flow drive population diversity of the brown alga \u003cem\u003eSargassum thunbergii\u003c/em\u003e along the coast of China. BMC Evol Biol. 2017;17:246.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMontecinos AE, Couceiro L, Peters AF, Desrut A, Valero M, Guillemin ML. Species delimitation and phylogeographic analyses in the \u003cem\u003eEctocarpus\u003c/em\u003e subgroup \u003cem\u003esiliculosi\u003c/em\u003e (Ectocarpales, Phaeophyceae). J Phycol. 2017;53(1):17\u0026ndash;31.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChen J, Zang Y, Liang S, Xue S, Shang S, Zhu M, et al. Comparative analysis of mitochondrial genomes reveals marine adaptation in seagrasses. BMC Genomics. 2022;23(1):800.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eStarko S, Bringloe TT, Gomez MS, Darby H, Graham SW, Martone PT. Genomic rearrangements and sequence evolution across brown algal organelles. Genome Biol Evol. 2021;13(7):evab124.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLiu F, Pan J, Zhang Z, Zhang ZS, Moejeset FW. Organelle genomes of \u003cem\u003eSargassum confusum\u003c/em\u003e (Fucales, Phaeophyceae): mtDNA vs cpDNA. J Appl Phycol. 2018;30:2715\u0026ndash;22.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eZhang SS, Liang YS, Zhang J, Draisma SGA, Duan D. Organellar genome comparisons of \u003cem\u003eSargassum polycystum\u003c/em\u003e and \u003cem\u003eS. plagiophyllum\u003c/em\u003e (Fucales, Phaeophyceae) with other \u003cem\u003eSargassum\u003c/em\u003e species. BMC Genomics. 2022;23(1):629.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVieira C, Steen F, D\u0026rsquo;hondt S, Bafort Q, Tyberghein L, Fernandez-Garc\u0026iacute;a C, et al. Global biogeography and diversification of a group of brown seaweeds (Phaeophyceae) driven by clade-specific evolutionary processes. J Biogeogr. 2021;48:703\u0026ndash;15.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVieira C, Camacho O, Sun Z, Fredericq S, Leliaert F, Payri C, et al. Historical biogeography of the highly diverse brown seaweed \u003cem\u003eLobophora\u003c/em\u003e (Dictyotales, Phaeophyceae). Mol Phylogenet Evol. 2017;110:81\u0026ndash;92.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGuiry MD, Guiry GM. 2023. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://www.algaebase.org\u003c/span\u003e\u003cspan address=\"https://www.algaebase.org\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e; searched on December 22, 2023.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNi-Ni-Win, Hanyuda T, Arai S, Uchimura M, Prathep A, Draisma SGA et al. A taxonomic study of the genus \u003cem\u003ePadina\u003c/em\u003e (Dictyotales, Phaeophyceae) including the descriptions of four new species from Japan, Hawaii, and the Andaman sea. 2011;47(5):1193\u0026ndash;209.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWichachucherd B, Prathep A. Preliminary study on the diversity and distribution of \u003cem\u003ePadina\u003c/em\u003e Adanson in Peninsular Thailand, including a new record, \u003cem\u003ePadina usoehtunii\u003c/em\u003e Ni-Ni-Win et Kawai. Inst Ocean Earth Sci Univ Malaya Monogr. 2013;15:175\u0026ndash;83.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWichachucherd B. Phylogeography of \u003cem\u003ePadina boryana\u003c/em\u003e (Dictyotales, Phaeophyceae) around the Thai-Malay Peninsula. Ph.D. dissertation Prince of Songkhla University, Hat Yai, Thailand. 2014;57 pp.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDeb B, Uddin A, Chakraborty S. Composition, codon usage pattern, protein properties, and influencing factors in the genomes of members of the family Anelloviridae. Arch Virol. 2021;166(2):461\u0026ndash;74.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKim H, Yang JH, Bustamante DE, Calderon MS, Mansilla A, Maggs CA, et al. Organelle genome variation in the red algal genus \u003cem\u003eAhnfeltia\u003c/em\u003e (Florideophyceae). Front Genet. 2021;12:724\u0026ndash;34.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLee JM, Song HJ, Park SI, Lee YM, Jeong SY, Cho TO, et al. Mitochondrial and plastid genomes from coralline red algae provide insights into the incongruent evolutionary histories of organelles. Genome Biol Evol. 2018;10(11):2961\u0026ndash;72.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSmith DR. Mutation rates in plastid genomes: they are lower than you might think. Genome Biol Evol. 2015;7(5):1227\u0026ndash;34.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSmith DR, Keeling PJ. Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc. Natl Acad Sci U S A. 2015;112(33):10177\u0026ndash;10184.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChoi JW, Graf L, Peters AF, Cock JM, Nishitsuji K, Arimoto A, et al. Organelle inheritance and genome architecture variation in isogamous brown algae. Sci Rep. 2020;10(1):2048.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMaier UG, Fraunholz M, Zauner S, Penny S, Douglas S. A nucleomorph-encoded CbbX and the phylogeny of RuBisCo regulators. Mol Biol Evol. 2000;17(4):576\u0026ndash;83.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMohanta TK, Khan A, Khan AL, Hashem A, Abd_Allah EF, Al-Harrasi A. Gene Loss and Evolution of the Plastome. Genes. 2020;11(10):1133.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHan KY, Maciszewski K, Graf L, Yang JH, Andersen RA, Karnkowska A, et al. Dictyochophyceae plastid genomes reveal unusual variability in their organization. J Phycol. 2019;55(5):1166\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKim JI, Shin H, Škaloud P, Jung J, Yoon HS, Archibald JM, et al. Comparative plastid genomes of Synurophyceae: inverted repeat dynamics and gene content variation. BMC Evol Biol. 2019;19(1):20\u0026ndash;33.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMar\u0026eacute;chal A, Brisson N. Recombination and the maintenance of plant organelle genome stability. New Phytol. 2010;186(2):299\u0026ndash;317.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGoulding SE, Olmstead RG, Morden CW, Wolfe KH. Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet. 1996;252(1\u0026ndash;2):195\u0026ndash;206.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCattolico RA, Jacobs MA, Zhou Y, Chang J, Duplessis M, Lybrand T, et al. Chloroplast genome sequencing analysis of \u003cem\u003eHeterosigma akashiwo\u003c/em\u003e CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics. 2008;9:211.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLommer M, Roy AS, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J. Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genomics. 2010;11:718.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBi YH, Feng B, Xie WY, Ouyang LL, Ye RX, Zhou ZG. Nuclear-encoded CbbX located in chloroplast is essential for the activity of red-type Rubisco in \u003cem\u003eSaccharina japonica\u003c/em\u003e. Plant Physiol Biochem. 2023;196:236\u0026ndash;45.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSmith DR, Arrigo KR, Alderkamp AC, Allen AE. Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of \u003cem\u003ePhaeocystis\u003c/em\u003e algae. Mol Phylogenet Evol. 2014;71:36\u0026ndash;40.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSmith DR, Hua J, Lee RW, Keeling PJ. Relative rates of evolution among the three genetic compartments of the red alga \u003cem\u003ePorphyra\u003c/em\u003e differ from those of green plants and do not correlate with genome architecture. Mol Phylogenet Evol. 2012;65:339\u0026ndash;44.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDrouin G, Daoud H, Xia J. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol. 2008;49:827\u0026ndash;31.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWang H, Meng T, Wei W. Analysis of synonymous codon usage bias in helicase gene from \u003cem\u003eAutographa californica\u003c/em\u003e multiple nucleopolyhedrovirus. Genes Genom. 2018;40(7):767\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114\u0026ndash;20.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAltschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403\u0026ndash;10.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKatoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTalavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56(4):564\u0026ndash;77.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268\u0026ndash;74.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGuindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307\u0026ndash;21.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMinh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30:1188\u0026ndash;95.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRonquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, H\u0026ouml;hna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539\u0026ndash;42.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMinh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30(5):1188\u0026ndash;95.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194\u0026ndash;202.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDarling AC, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394\u0026ndash;403.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLi H, Guo Q, Xu L, Gao H, Liu L, Zhou X. CPJSdraw: analysis and visualization of junction sites of chloroplast genomes. PeerJ. 2023;11:e15326.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eZhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, et al. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 2020;20(1):348\u0026ndash;55.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKatoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTalavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56(4):564\u0026ndash;77.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eYang Z. PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24(8):1586\u0026ndash;91.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBeier S, Thiel T, M\u0026uuml;nch T, Scholz U, Mascher M. MISA-web: a web server for microsatellite prediction. Bioinformatics. 2017;33(16):2583\u0026ndash;5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKurtz S, Schleiermacher C. Reputer: fast computation of maximal repeats in complete genomes. Bioinformatics. 1999;15(5):426\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePeden JF. Analysis of codon usage. Univ Nottm. 2000;90(1):73\u0026ndash;4.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBehura SK, Severson DW. Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS ONE. 2012;7(8):e43111.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-genomics","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"gics","sideBox":"Learn more about [BMC Genomics](http://bmcgenomics.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/gics","title":"BMC Genomics","twitterHandle":"#BMCGenomics","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Padina usoehtunii, Dictyotales, Phaeophyceae, chloroplast genome, mitochondrial genome, phylogeny, structural variation, sequence variation","lastPublishedDoi":"10.21203/rs.3.rs-3835960/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3835960/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eOrganellar genomes have become increasingly essential for studying genetic diversity, phylogenetics, and evolutionary histories of seaweeds. The order Dictyotales (Dictyotophycidae), an early-diverging and highly diverse lineage within the Phaeophyceae, is long-term characterized by a scarcity of organellar genome datasets compared to orders of the brown algal crown radiation (Fucophycidae).\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eWe sequenced the organellar genomes of \u003cem\u003ePadina usoehtunii\u003c/em\u003e, a representative of the order Dictyotales, to investigate the structural and evolutionary differences by comparing to five other major brown algal orders. Our results confirmed that the rate of structural rearrangements in chloroplast genomes is higher than that in mitochondria, whereas mitochondrial sequences exhibited a higher substitution rate compared to chloroplasts. Such evolutionary patterns contrast with land plants and green algae. The expansion and contraction of the inverted repeat (IR) region in the chloroplast correlated with the changes in the number of boundary genes. Specifically, the size of the IR region influenced the position of the boundary gene \u003cem\u003erpl\u003c/em\u003e21, with complete \u003cem\u003erpl\u003c/em\u003e21 genes found within the IR region in Ectocarpales, while the \u003cem\u003erpl\u003c/em\u003e21 genes in Desmarestiales, Fucales, and Laminariales span both the IR and short single copy (SSC) regions. The absence of the \u003cem\u003eRbc\u003c/em\u003eR and \u003cem\u003erpl\u003c/em\u003e32 genes in the Dictyotales may indicate a horizontal transfer from the chloroplast to the nuclear genome. Inversion of the SSC region occurred at least twice in brown algae. Once in a lineage only represented by the Ectocarpales in the present study and once in a lineage only represented by the Fucales. Photosystem genes in the chloroplasts experienced the strongest purifying selection, while ribosomal protein genes in both chloroplasts and mitochondria underwent a weak purifying selection.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eVariations in chloroplast genome structure among different brown algal orders are evolutionarily linked to their phylogenetic positions in the Phaeophyceae tree. Structural variability to some extent is an inherent mechanism to create genetic diversity of brown algal taxa. Different functional gene categories in organelles exhibit varying degrees of structural variation and distinct patterns of sequence evolution, potentially giving rise to new genes adapted to various environmental pressures.\u003c/p\u003e","manuscriptTitle":"Comparative structure and evolution of the organellar genomes of Padina usoehtunii (Dictyotales) with the brown algal crown radiation clade","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-11 09:19:25","doi":"10.21203/rs.3.rs-3835960/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-02-06T06:11:51+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-02-03T18:26:09+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"04ab3b08-e4d8-4be4-8c02-35bf692a1ac1","date":"2024-01-23T23:45:48+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-01-23T16:35:14+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-01-19T08:02:48+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2024-01-09T10:53:03+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-01-09T10:47:57+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Genomics","date":"2024-01-05T02:38:08+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-genomics","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"gics","sideBox":"Learn more about [BMC Genomics](http://bmcgenomics.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/gics","title":"BMC Genomics","twitterHandle":"#BMCGenomics","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"f1cfdc66-18a6-45b1-9f6a-a6b06310cb2b","owner":[],"postedDate":"January 11th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-08-05T16:05:34+00:00","versionOfRecord":{"articleIdentity":"rs-3835960","link":"https://doi.org/10.1186/s12864-024-10616-4","journal":{"identity":"bmc-genomics","isVorOnly":false,"title":"BMC Genomics"},"publishedOn":"2024-07-31 15:57:56","publishedOnDateReadable":"July 31st, 2024"},"versionCreatedAt":"2024-01-11 09:19:25","video":"","vorDoi":"10.1186/s12864-024-10616-4","vorDoiUrl":"https://doi.org/10.1186/s12864-024-10616-4","workflowStages":[]},"version":"v1","identity":"rs-3835960","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3835960","identity":"rs-3835960","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}