Maize and wild relatives show distinct patterns of genome downsizing following polyploidy

Maize and wild relatives show distinct patterns of genome downsizing following polyploidy | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (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];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Maize and wild relatives show distinct patterns of genome downsizing following polyploidy View ORCID Profile Samantha J. Snodgrass , Margaret Woodhouse , View ORCID Profile Arun Seetharam , View ORCID Profile Michelle Stitzer , View ORCID Profile Matthew B. Hufford doi: https://doi.org/10.1101/2024.12.24.630189 Samantha J. Snodgrass 1 Department of Ecology, Evolution, and Organismal Biology, Iowa State University , Ames, IA 4 Evolution and Ecology Department, University of California Davis , Davis, CA Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Samantha J. Snodgrass Margaret Woodhouse 3 USDA-ARS, Corn Insects and Crop Genetics Research Unit , Ames, IA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Arun Seetharam 1 Department of Ecology, Evolution, and Organismal Biology, Iowa State University , Ames, IA 2 Department of Genetics, Development, and Cellular Biology, Iowa State University , Ames, IA Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Arun Seetharam Michelle Stitzer 5 Institute for Genomic Diversity, Cornell University , Ithaca, NY Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Michelle Stitzer Matthew B. Hufford 1 Department of Ecology, Evolution, and Organismal Biology, Iowa State University , Ames, IA Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Matthew B. Hufford For correspondence: mhufford{at}iastate.edu Abstract Full Text Info/History Metrics Supplementary material Data/Code Preview PDF Abstract Plant genomes are smaller than expected despite the ubiquity of polyploidy due to the process of genome downsizing called fractionation. This process causes loss of DNA sequences, including genes, until genomes return to a diploid-like state, though some duplicates remain from the polyploid ancestor. Fractionation can affect the copies of ancestral diploid genomes ( i.e. , subgenomes) differently, resulting in one being preferentially retained and the other preferentially lost. While previous work suggested fractionation occurs shortly after a polyploidy event, few studies have been able to densely sample descendent genomes from the same whole genome duplication event. The Tripsacinae subtribe of grasses, which includes the genera Tripsacum and Zea and the economically and culturally important maize ( Zea mays ssp. mays ), originates from an ancient allopolyploid (∼5-12 MYA). We use publicly available genome assemblies from the Tripsacinae subtribe of grasses to investigate the patterns and timing of fractionation relative to the outgroup sorghum, which does not share the allotetraploidy event. Our results show the majority of fractionation following polyploidy occurred in a common ancestor of modern species and that one subgenome is preferentially retained, in keeping with previous studies of maize. However, Tripsacum retains a greater proportion of duplicate genes (homoeologs) than Zea , potentially related to the fewer chromosomal rearrangements observed in this genus. Multiple, nested deletion events were commonly observed in alignments to a single sorghum reference exon, and some homoeologs show fractionation of different exons across genomes. Further, ∼35% of homoeologous pairs of exons show differential fractionation, where fractionation patterns differ between species. Altogether, this suggests multiple origins of fractionation for a given homoeolog may be common. We demonstrate that fractionation is a much more dynamic process in the Tripsacinae than previously predicted. Introduction Polyploidy, or whole-genome duplication (WGD), instantly inflates genome size and replicates every gene, regulatory sequence, and repetitive element from the parental genomes. Despite the frequency of polyploidy ( Wendel et al., 2016 ), smaller than expected genome sizes predominate in angiosperms ( Knight, 2005 ). This suggests larger genomes face pressure to undergo sequence loss, or fractionation, with proposed selective pressures ranging from nutrient limitation, effects on growth rate, and other higher-order biological processes (for a more comprehensive review, see Escudero & Wendel, 2020 ; Faizullah et al., 2021 ; Wendel, 2015 ). Descendant, duplicate copies of a gene are homoeologs. While they may begin as a pair after the WGD, one or both homoeologs may be fractionated over time. Homoeologs from one subgenome may be preferentially lost, a phenomenon known as biased fractionation ( Thomas et al., 2006 , Wendel et al., 2018 , Li et al., 2022). Within the Andropogoneae tribe of grasses is the Tripsacinae subtribe which originates from an ancient whole genome duplication (WGD) that occurred approximately 5 – 12 million years ago ( Gaut & Doebley, 1997 ; Schnable et al., 2011 ; Swigoňova et al., 2004 ; Woodhouse et al., 2010 ). The subtribe consists of two genera, Tripsacum (haploid chromosome n=18, Anderson 1944 , Maguire 1961 ) and Zea (haploid chromosome n=10), which includes the globally important crop, maize ( Zea mays ssp. mays ). Almost all Zea species and roughly half of Tripsacum species are cytologically diploid, with all current polyploids the product of subsequent rounds of WGD (Cutler et al., 1941, Li et al., 1999 , Pasupuleti and Galinat 1982). The Tripsacinae polyploidy event occurred through the hybridization of an ancient species similar to modern Urelytrum and Vossia and another species similar to modern Rottboellia-Hemarthria ( McKain et al., 2016 ). Alignment of any diploid species of the Tripsacinae to close relatives which did not undergo the Tripsacinae WGD ( e.g. , Sorghum bicolor (sorghum) or Anatherum virginicum ) results in two orthologous, syntenic regions from the Tripsacinae genome aligned to one region in the unduplicated species (Schnable et. al. 2011; Lovell et. al. 2022). Zea species show strong synteny and collinearity to each other but extensive chromosomal rearrangements when aligned to other grasses such as sorghum (Schnable et. al. 2011; Chia et. al. 2012; Lovell et. al. 2022). While limited work has shown some synteny between Tripsacum and Zea ( Galinat 1973 ), the extent of synteny has not been analyzed via comparative genomics. Previous studies predict that fractionation patterns will be similar ( i.e., which homoeologs are lost, amount of loss) between descendents of the same WGD event, but this has yet to be measured directly in the Tripsacinae ( Gault et al., 2018 ; Sankoff et al., 2010 ). Until recently, fractionation studies of this subtribe have focused primarily on domesticated maize, finding most homoeologs have either been reduced to single copy or experienced partial loss across genomes (∼43% and ∼16% respectively, Hufford et al., 2021 ). Biased fractionation by small deletion events identified in Zea mays ssp. mays B73 (Zm B73) affected maize subgenome 2 (M2) more than maize subgenome 1 (M1) ( Schnable et al., 2011 ; Woodhouse et al., 2010 ). SNPs in M1 regions of the maize genome show greater association with phenotypic variability across traits than M2 ( Renny-Byfield et al., 2017 ) suggesting the M1 subgenome retains more function. Comparisons between two temperate maize genomes found little differential fractionation ( i.e. , where different homoeologs of a gene are fractionated between genomes), suggesting fractionation had occurred before divergence of these lines ( Brohammer et al., 2018 ). When expanded to include more diverse maize assemblies, more diverged lines had fewer fractionation events in common, suggesting more ongoing fractionation than previously observed ( Hufford et al., 2021 ). Further, approximately 200 cases were identified where the same homoeolog was fractionated but different exons were lost across these diverse genomes, suggesting multiple origins of fractionation (personal correspondence with M. Woodhouse). Ongoing fractionation at such recent time scales contrasts with the prevailing hypothesis that most fractionation occurs shortly after a WGD event ( Schnable et al., 2011 ). Rapid loss of homoeologs has been observed in the aftermath of other WGD events across a wide breadth of systems, including angiosperms ( Li et al., 2016 ), Brassica napus ( Szadkowski et al., 2010 ), Paramecium , Arabidopsis , vertebrates, yeast, and teleosts ( Sankoff et al., 2010 ). Yet in other lineages like Brachypodium , homoeologs have been retained for long periods of time and show gradual loss ( Scarlett et al., 2023 ). Given limited genomic resources for the wild species of the subtribe, patterns of fractionation and their relationship to lineage divergence within the Tripsacinae have not been studied. This study uses the recent publicly available high quality pseudomolecule assemblies of wild Zea species and Tripsacum in conjunction with the existing and publicly available maize NAM genomes to investigate the timing and patterns of exon fractionation relative to the sorghum outgroup in the Tripsacinae ( Stitzer et al., 2024 ; Hufford et al 2021 ). By including the wild Tripsacinae species, we investigate fractionation at larger divergence times than between any two maize accessions (∼650 KYA between Tripsacum and Zea to ∼67 KYA between Zea mays subspecies, Chen et al 2022 ). - We observe less extensive fractionation in Tripsacum relative to Zea, suggesting fractionation in Zea continued to a greater extent after the genera diverged. Otherwise, Zea genomes share fractionation patterns across most exons, indicating a large proportion of fractionation occurred before these species diverged. However, some differences between Zea species, subspecies, and accessions were observed, suggesting recent fractionation at low levels. In total, ∼35% of homoeologous pairs of exons relative to sorghum show differential fractionation, where the fractionation pattern of a pair of homoeologous exons differs across species, subspecies, or accessions. Altogether, we demonstrate that fractionation is a much more dynamic process in the Tripsacinae than previously predicted. Materials and Methods Data The recent publicly available pseudomolecule assemblies for two Zea mays ssp. mexicana accessions (Zx), two Zea mays ssp . parviglumis accessions (Zv), one Zea mays ssp. huehuetenagensis accession (Zh), two Zea diploperennis accessions (Zd), one Zea nicaraguensis accession (Zn), two Tripsacum dactyloides accessions (Td), and one Anatherum virginicum accession ( Stitzer et al., 2024 ) were used in conjunction with the existing NAM Zea mays ssp. mays genomes (26 accessions, Zm). Sorghum bicolor 313 (sorghum) ( McCormick et al., 2017 ) and Anatherum virginicum ( Stitzer et al., 2024 ) are similar phylogenetic distances from the Tripsacinae and used as outgroup species. Creating alignments Based on segment length and number of aligned segments, we filtered syntenic orthologous regions identified by GENESPACE ( Lovell et al., 2022 ) that did not match the expected 2:1 relationship arising from the Tripsacinae WGD. Small regions around 1MB in length and deviating from this expectation (3 or more to 1) were removed as likely remnants from an older WGD that is shared by Poaceae , which includes the Tripsacinae and sorghum ( Paterson et al., 2004 ). Due to low mapping quality for the Z. nicaraguensis and Z. diploperennis genomes, likely driven by assembly artifacts of highly heterozygous individuals, those genomes were also remapped with an expected 4:1 alignment relative to sorghum. Only one known translocation was observed within the Zea genus ( Z. mays ssp mays Oh7B) with otherwise strongly conserved synteny within genera. Given the strong synteny, we manually assigned subgenomes to individual Zea orthologous syntenic regions based on their synteny with sorghum using the subgenome assignments created by Schnable et al (2011) . We used the syntenic regions identified by GENESPACE (Lovell et. al., 2022) between each Tripsacum genome and Zm B73 to manually assign subgenome identity. For example: Tripsacum chr13 is syntenic to sorghum Chr10 and Zm B73 chr6. Given the region of B73 chr6 syntenic to sorghum Chr10 is assigned the M2 subgenome, the Tripsacum chr13 is assigned to M2 where it is syntenic to sorghum Chr10. The same process was used to resolve the subgenome assignment of the translocation in Zm Oh7b. Each Tripsacinae genome was aligned to sorghum using AnchorWave ( Song et al., 2022 ) with sorghum as reference and parameters -R 2 and -Q 1. For Z. nicaraguensis and Z. diploperennis , additional alignments were made with -R 4 and -Q 1 (labeled 4to1 throughout). Resulting MAFs were split first by Tripsacinae sequence name and then by the sorghum sequence name using mafSplit ( Perez et al., 2024 ). Using subgenome identity assigned to each Tripsacinae -sorghum chromosome pair, the split MAFs were concatenated by subgenomes into “Bin1” and “Bin2” MAF files corresponding to the M1 and M2 subgenomes, respectively. These concatenated subgenome MAFs were converted to GVCF using the MAFToGVCF phg plugin ( Bradbury et al., 2022 ). GVCFs’ alignment quality was evaluated by VCFMetricsPlugin ( Bradbury et al 2007 ). To remove any potential lineage-specific sorghum exons, we identified a set of conserved gene models to use for all downstream analyses. This gene set was identified through reciprocal liftover of sorghum 313 and A. virginicum annotations using Liftoff ( Shumate and Salzberg 2021 ). Sorghum and A. virginicum annotations with the exact same exon structures (exact same exon number and exon lengths) were kept as outgroup reference exons (12,157 genes, 69,269 exons). Categorizing deletions For each sorghum chromosome, M1 and M2 GVCFs were combined across all genomes except Z. nicaraguensis to create a VCF using GATK GenomicsDBImport and GenotypeGVCFs tools ( Van der Auwera and O’Connor 2020 ). VCFs were filtered for indel variants using GATK SelectVariants ( Van der Auwera and O’Connor 2020 ) and reformatted using bcftools annotate ( Danecek et al., 2021 ). Custom scripts further filtered insertion variants and converted the VCF to bed format. Lengths of deletions were calculated as the length of the REF allele minus the length of the ALT allele to create end coordinates. Further filtering of deletions left only those intersecting reference exons as “exonic deletions” using bedtools intersect ( Quinlan and Hall 2010 ). Deletions that reciprocally overlap each other at least 80% were collapsed. Collapsed deletion genotypes were called based on the genotypes of all deletions being collapsed. New genotypes for reference correspond to only “0” genotypes, alternative if at least one deletion was genotyped “1”, and NA or “.” if no call was made. Calling fractionation status AnchorWave ( Song et al., 2022 ) guides alignment by identifying syntenic blocks, and thus regions beyond syntenic blocks may not be aligned and thus not included in the GVCF. To identify reference exons that were aligned, each GVCF was converted to a bed file by a custom script and then intersected with the sorghum reference exon bedfile using bedtools2 ( Quinlan and Hall 2010 ). Exons within the GVCF-derived bed file were classified as “aligned” and all others as “unaligned”. All genomes were checked to make sure that the number of aligned and unaligned exons summed to the total 69,269 exons. Each GVCF-derived bed file was filtered for deletions, defined as the length of the reference allele being longer than the length of an alternative allele that was not . Deletion lengths were assigned as the length of the reference allele minus the length of the alternative allele. These deletions’ coordinates were intersected with the aligned exons for that GVCF ( Quinlan and Hall 2010 ). If the aligned reference exon intersected with at least one deletion, that exon was called “fractionated”. Otherwise, the exon was assigned “retained”. Each set of retained and fractionated calls by genome and subgenome was joined by CDS ID using a custom R script (“fractionation-calling.R”) to create a dataframe where each row indicated a reference exon, each subgenome of each query genome was a column, and the value within each cell referred to fractionation status (0 = retained, 1 = fractionated, NA = unaligned). For analyses summarizing fractionation of an entire gene, multiple cutoffs were used of varying stringencies. The broadest was at least one exon called fractionated (“at least one” or “only1”) and the strictest required all exons to be fractionated (“all”). Between these two cutoffs were at least ⅓ or ½ of the exons called fractionated (“⅓” or “third” and “½” or “half” respectively). For all cutoffs, if a gene did not meet the cutoff for fractionation calling, it was considered retained. To estimate the amount of a homoeolog being fractionated, we calculated the number of exons called fractionated out of the total exons within the homoeolog. There was a significantly larger percentage of unaligned exons within Z. nicaraguensis and Z. diploperennis compared to other Tripsacinae genomes. These genomes were assembled from heterozygous individuals and contain multiple haplotypes. Increasing the alignment ratio from 2:1 to 4:1 did align thousands more exons for each Z. diploperennis genomes (Zd Gigi = 2933, ZdMomo = 5241), but only 341 more exons for Z. nicaraguensis. This is likely due to the comparatively more fragmented nature of the Z. nicaraguensis genome assembly rather than biological differences. Given that Z. diploperennis genomes had better alignments overall that were substantially improved compared to Z. nicaraguensis , the “4to1” Z. diploperennis alignments were used in all downstream analyses, but Z. nicaraguensis was removed. Agreement between fractionation calls using the GVCFs versus the VCFs as the input files was evaluated. Because the combined VCFs only include information on deletions and not retention of sequences, comparisons are difficult to interpret as either true disagreements or missing information could lead to a disagreement in classifications. However ∼73% of calls agree between methods. All scripts for this analysis can be found at: https://github.com/Snodgras/Zea_Fractionation Convergence of fractionation by gene The exons called fractionated for a given homoeolog were compared between two genomes. Homoeologs where any exon was unaligned were ignored for this analysis. If all of the exons that were called fractionated in each genome were the same, that homoeolog was considered “Completely Shared”. If none of the fractionated exons were the same, either because completely different exons were fractionated, the homoeolog was considered “Completely Different”. If all exons were shared or different due to both or one genome fully retaining a homoeolog respectively, the suffix “Ret.” was added to parse similarities and differences caused by retention from those solely by fractionation. If some exons shared fractionation status, but not all, the homoeolog was considered “Some Shared”. This was done for each pair of genomes and each individual homoeolog. Spatial organization of fractionation For each sorghum reference chromosome, the counts of homoeologous exon pairs in each fractionation status category (“Both Retained”, “Both Deleted”, “M1 Retained”, “M2 Retained”) was calculated. Percentages were calculated by count of exons within a category/total number of exons on a given sorghum reference chromosome. The significance of differences in percent exons in each category across sorghum reference chromosomes was evaluated using an ANOVA. Tempo of Fractionation The timing of each fractionation event was estimated relative to the phylogeny of the query genomes, which was created from ( Stitzer et al., 2024 ) and previous phylogenies ( Hufford et al., 2012 ; Hufford et al., 2021 ). Under the assumption of parsimony, exons retained in all genomes outside a monophyletic branch and fractionated in all genomes within that monophyletic branch were assigned to that node for the relative timing of loss. Exons that exhibited non-monophyletic patterns were not assigned a time point and classified as “paraphyly”. Exons must be aligned to be included. For those exons that show non-monophyletic patterns of fractionation, we create a “paraphyly pattern” which is a string with the names of the genomes that show fractionation of that exon. These patterns can include 2 to 34 genomes. Gene Ontology Analysis Gene ontology enrichment analysis was performed using the PANTHER database tools ( Thomas et al., 2022 ). We used the PANTHER GO-Slim categories as they are more manually curated and of higher confidence than the broader GO categories for the three domains: biological, cellular, and molecular processes. We used our set of ∼12K highly conserved genes as the reference list instead of all the genes within the reference sorghum gene annotation. Fisher’s exact test with false discovery rate p-value adjustments were used for all tests. dN/dS Analysis dN/dS measures of B73 M1 and M2 to Sorghum from Yin et al. (2022) were used. Genes within both our reference set and the Yin et al. (2022) set were used to compare dN/dS across various categories of genes, particularly those related to convergence across genomes. Results Chromosomal rearrangements differ in Tripsacum and Zea All Tripsacinae genomes had two sets of detectable syntenic orthologous blocks relative to sorghum genome-wide ( Figure 1 ). Tripsacum showed fewer ancestral translocations relative to Zea (at least two ancestral chromosomes broken and incorporated across two Tripsacum chromosomes) among the 18 modern chromosomes: 14 Tripsacum chromosomes comprise a full syntenic copy of a sorghum chromosome ( Figure 1 ). In contrast, Zea shows abundant ancestral chromosomal translocations and structural rearrangements such that 9 out of 10 modern Zea chromosomes are mosaics relative to sorghum chromosomes (at least 5 ancestral chromosomes broken and fused such that each modern chromosome has fragments from 2-4 different ancestral chromosomes, Supp. Figure 1 ). Only Zea chromosome 7 shows synteny to a single sorghum chromosome ( Figure 1 ). All Zea genomes show strong synteny and collinearity at the chromosome level, though there are inversion polymorphisms within chromosomes. The one exception is a known translocation from chromosome 10 to chromosome 9 in Zm Oh7b ( Hufford et al., 2021 ). The same translocations in Tripsacum are also detected in Zea , suggesting those rearrangements occurred before the divergence of the two genera. Likewise, the numerous rearrangements shared across the Zea genomes likely happened before speciation in the Zea genus. Download figure Open in new tab Figure 1. Riparian plot between all genomes. Colored braids show syntenic blocks between genomes, colored by sorghum reference chromosome. Twists in the colored braids indicate inversions between genomes. Genome species from bottom to top: Anatherum virginicum (Av), Sorghum bicolor (Sb313), Tripsacum dactyloides (Td FL, Td KS), Zea nicaraguensis (Zn PI615697), Zea diploperennis (Zd Momo, Zd Gigi), Zea mays ssp. huehuetenagensis (Zh RIMHU001), Zea mays ssp. mexicana (Zx TIL25, Zx TIL18), Zea mays ssp. parviglumis (Zv TIL01, Zv TIL11), and Zea mays ssp. mays (Tropical: Zm Tzi8, Zm NC358, Zm NC350, Zm Ki3, Zm Ki11, Zm CML69, Zm CML52, Zm CML333, Zm CML322, Zm CML277, Zm CML247, Zm CML228, Zm CML103. Mixed: Zm Tx303, Zm Mo18W, Zm M37W. Temperate + Sweet corn + Popcorn: Zm P39, Zm HP301, Zm Oh7b, Zm Oh43, Zm MS71, Zm M162W, Zm Ky21, Zm IL14H, Zm B97, Zm B73) Multiple deletions underlie most fractionation calls at the exon and gene level For a given exon, multiple polymorphic and possibly overlapping deletions occur, obscuring separate deletions as a single event. The percentage of deletions nested in other deletions is high across both subgenomes (∼30-50%) while the percentage of exons with a single deletion event is < 10% ( Figure 2 ). While more than 2/3 of exonic deletions were smaller than the exon itself, around 25% of deletions intersected with multiple exons. Given the difficulty of pinpointing distinct deletion events at the resolution of a single exon or even a single gene, we define an exon as fractionated if any deletion overlaps its boundaries. Download figure Open in new tab Figure 2. Deletion descriptions that intersect with reference exon alignments. A) Each point represents the counts of base pairs that overlap with a deletion called for a given exon or gene in a genome plotted against the length of the exon or gene. The black diagonal line is 1:1. B) Heatmap of counts of the variant types paired together as two alt alleles of the same variant in the VCF. Lighter colors are more common. C) Counts of deletions within each size class, separated by deletions that were 80% reciprocally overlapping (collapsed del.) and those that were distinct (deletions). Tripsacum retains more exons and genes than Zea Of the 69,269 sorghum- A. virginicum exons aligned from Tripsacum and Zea , over 50% are retained as a singleton while the remaining exons are evenly split between both retained or lost ( Figure 3 , Table 1 , 2 ). Homoeologous pairs of exons where at least one exon is unaligned comprise less than 10% of exons on average. Tripsacum has more retained exons and better alignment to sorghum than do the Zea genomes, particularly Td FL ( Supp. Figure 2 ). Across all genomes, the M1 homoeologous exon is more often retained than the M2 homoeologous exon ( Supp. Figure 3 ). This supports preferential fractionation in M2, which has been demonstrated previously ( Schnable et al 2011 , Hufford et al 2021 , Stitzer et al., 2024 ). Download figure Open in new tab Figure 3. Fractionation Status by Genome. Status categories reflect if homoeologous exons (A) or genes (B) are both retained, both lost, only one is retained by each genome, or if at least one of the exons is unaligned (NA). Points represent genomes and are colored by broad taxonomic classifications. Percentages refer to the number of reference exons per genome fitting a particular category out of the 69,269 total reference exons or 12,169 reference genes. Underlying violin plots represent the overall distribution across the Tripsacinae . The Z. nicaraguensis genome is excluded. B) Panels show different cutoffs for calling a gene fractionated based on the number of exons within a homoeolog called fractionated. View this table: View inline View popup Table 1. Counts of reference exons of each fractionation status across all genomes. Included are the counts for Zea nicaraguenesis and Zea diploperennis with both standard 2:1 and 4:1 alignments to Sorghum. Total reference exons is 69269. View this table: View inline View popup Table 2. Percentages of reference exons of each fractionation status across all genomes. Included are the counts for Zea nicaraguenesis and Zea diploperennis with both standard 2:1 and 4:1 alignments to Sorghum. Rounded to 2 decimal places. Gene fractionation was called across four different cutoffs varying in stringency. These ranged from the broadest, in which at least one exon out of the gene model was called fractionated for the homoeolog, to the most conservative, in which all exons of a gene model must be called fractionated. As expected, the number of homoeologs called fractionated across genomes decreases with cutoff stringency for both subgenomes ( Figure 3 B). Across cutoffs, M2 had a higher percentage of genes fractionated than M1, even at the most conservative cutoff (M1 mean =42.6%, M2 mean =55.2%). Patterns of fractionation ( e.g., “Both Retained”, “Both Lost”, “M1 Retained”, “M2 Retained”) mirrored the results at the exon level where M1 is retained in singleton more than M2 and Tripsacum genomes retain more homoeologs as pairs than Zea genomes ( Figure 3 ). Within a given gene, no matter the genome or subgenome, most exons are fractionated ( Supp. Figure 4 , Figure 3 ). However, there are slight but significant differences between subgenomes (p < 2e-16) and across genomes (p < 2e-16). M2 homoeologs lost ∼10% more exons compared to M1 homoeologs. Zea on average lost ∼2.51-2.88% more exons from a gene compared to Tripsacum ( Supp. Figure 4 ). Differences in the amount of exons lost between M1 and M2 homoeologs were similar in pairwise comparisons of Zea genomes ( Supp. Figure 4 A). Amount of fractionation varies by sorghum reference chromosome Given the conserved synteny and collinearity between Andropogoneae genomes ( Stitzer et al., 2024 ), we assume that the ancestral polyploid chromosome structure can be modeled by the modern assembly of sorghum in duplicate. Thus, if fractionation occurred evenly across ancestral chromosomes, the proportion of exons in each fractionation category should be similar across the sorghum reference chromosome. However, we found significant differences in the proportion of exons by fractionation category across sorghum reference chromosomes ( Figure 4 ). In general, reference chromosomes that show a large number of rearrangements in the Tripsacinae ( e.g. , sorghum chromosomes 5 and 7) or those that are smaller ( e.g., sorghum chromosomes 8 through 10) tend to show more fractionation of either both or one copy of an exon compared to reference chromosomes that have remained more intact or are larger ( e.g. , sorghum chromosomes 1 through 3). For example, sorghum chromosome 1 has twice the average percentage of exons (mean =22.9%) in the “both retained” category as sorghum chromosome 5 (mean =11.4%), and syntenic regions of sorghum chromosome 5 show the greatest number of structural rearrangements in Zea across both subgenomes (M1 is in at least 4 pieces, M2 is in 2, Figure 1 , Supp. Figure 1 ). Sorghum reference chromosomes 7 (M1 in at least 3 pieces across 3 Zea chromosomes, Figure 1 , Supp. Figure 1 ) and 10 (the smallest chromosome) show the highest percentages of exons categorized as “both deleted” while Sorghum reference chromosomes 1, 2, 3, 4, and 6 have the highest percentages of exons categorized as “both retained”. There are exceptions, such as the high percentage of M1 retained exons on sorghum reference chromosome 10. In general, these fractionation differences between ancestral chromosomes suggest a spatial context to fractionation. Download figure Open in new tab Figure 4. Fractionation status of exons by reference chromosome. For each fractionation category, the percentage of exons of a given sorghum reference chromosome in that category across Tripsacinae genomes is depicted. Letters indicate statistical differences between reference chromosomes in the same category. Zea nicaraguensis and Zea diploperennis assemblies are excluded. Differential fractionation across genomes A homoeolog is called differentially fractionated when it is retained in some genomes and fractionated in others, which has been observed in small amounts between relatively recently diverged maize accessions ( Brohammer et al., 2018 ; Hufford et al., 2021 ). We cataloged the number of homoeologous pairs of exons where the pair had the same fractionation status across all genomes (1 status: both retained, M1 retained, M2 retained, or both lost) or multiple (combinations of at least two of any of the previous status categories). Based on previous work ( Brohammer et al, 2018 ), we expected there to be minimal amounts of exons in the most differentially fractionated categories, where either multiple status categories are observed or the statuses observed completely oppose each other ( e.g., both retained and both lost being observed across genomes). Our observations follow these expectations, with the majority of homoeologous exon pairs fitting into a single status category across all genomes (∼60%) ( Figure 4 C). Observation of homoeologous exons showing multiple status categories across genomes drops by an order of magnitude between single and two status categories and from two to three or all status categories. Of those exons that are found to have 2 fractionation statuses called across genomes, ∼33% (7093 exon pairs) are differences between the Tripsacum accessions and Zea accessions. While exons with three and all observed statuses are a limited percentage of the total (∼3% and ∼ 1% respectively), these highly differentially fractionated categories represent hundreds of exons (2,539 exons and 555 exons respectively) which represent hundreds of genes (1,187 and 235 genes respectively). Genes which had exons that were the most differentially fractionated across genomes were not statistically enriched or depleted for GO terms, with one exception. Genes with exons with three statuses across genomes were enriched for cellular GO terms related to organellar and cytoplasmic membranes. Genes which had more conserved exon fractionation status, i.e. , only a single status across genomes, showed significant GO term enrichment across a variety of biological, molecular, and cellular processes. Briefly, genes with exons “both lost” were enriched for transcription factor related terms; genes with exons “both retained” were enriched for terms related to protein binding, regulation, and modifications; genes with exons “M1 retained” were enriched for terms related to nuclease activity but depleted for terms related to transcription factor binding; and genes with exons “M2 retained” were enriched for catalytic activity and vesicle related terms (Supplemental Data 1). At the gene level, many homoeologs show loss of the same exons across all genomes ( Supp. Figure 5 , Supp. Figure 6 ). Yet, some homoeologs show fractionation of different exons across genomes. In pairwise comparisons of genomes, a homoeolog could have complete sharing or difference of fractionation status due to both or one being completely retained. If fractionation has occurred for exons of the homoeolog in both genomes, the exons called fractionated could be all the same (“Completely Shared”), some but not all the same (“Some Shared”), or completely different (“Completely Different”). Homoeologs which only share some or none of the fractionated exons across genomes may provide evidence of multiple origins of fractionation and possibly convergence for a homoeolog towards fractionation. The vast majority of homoeologs (∼91%) across both M1 and M2 show complete sharing of fractionation across all genome pairs ( Figure 5 B, Supp. Figure 6 ). Significantly more homoeologs fractionate only some or completely different exons in pairwise comparisons between Tripsacum and Zea genomes ( Figure 5 B, Supp. Figure 6 ). Additionally, there are significantly more homoeologs that show only some sharing of exon fractionation in comparisons of Zea genomes across species and subspecies compared to comparisons of accessions ( Figure 5 B). Download figure Open in new tab Figure 5. Convergence of gene fractionation. A) Percentage of exons showing differential fractionation patterns across genomes. Colored boxes next to black dots represents the combinations of statuses observed. B) Percentage of genes that show either complete sharing or completely no sharing due to similarities or differences in gene retention (categories starting with “Ret.”) and games showing either complete, some, or no sharing of exons experiencing fractionation in pairwise comparisons between genomes. Comparisons are roughly grouped by taxonomic differences between genomes being compared ( i.e., genomes are both Zea species but not the same Zea species for “Zea_species”). Different letters represent significant differences. C and D) M1 and M2 dN/dS from ( Yin et al., 2022 ) from convergence categories where both pairwise compared genomes show some fractionation of a gene. Of homoeologs across these categories of fractionation sharing, the subset of genes within the dN/dS dataset from Yin et al. (2022) show a dN/dS distribution much less than 1, though with long tails ( Supp. Figure 7 ). Though the distributions differ by genomes, generally the more shared homoeologs show lower dN/dS than the more differently fractionated homoeologs ( Supp. Figure 7 ). This could also be a reflection of the different numbers of homoeologs across categories, with many more homoeologs per genome showing “complete sharing” than “some shared” than “completely different” (M1: 9058, 2460, 251; M2: 7090, 1765, 134 genes respectively). Most fractionation occurred before or just after genera diverged If a given exon is fractionated across a monophyletic clade of genomes, we assume the deletion of the exon occurred in that clade’s most recent common ancestor. This assumption could be violated if a given exon has multiple deletion origins; for instance, one deletion in some genomes is on the 3’ end of an exon, while another deletion in other genomes is on the 5’ end of an exon. Only sorghum reference exons which aligned across all genomes were used to estimate timing, which corresponds to 59,164 M1 exons and 44,321 M2 exons. The majority of exons (∼80%) are either completely retained or fractionated across the entire Tripsacinae for both M1 and M2 ( Figure 6 ). However, M1 shows more complete retention than M2 (51.9% vs 34.2% respectively). Between genera, more exons are fractionated in Zea vs. Tripsacum (3.54% vs. 1.31% in M1, 4.8% vs. 1.05% in M2). The amount of fractionation observed at more recent timescales ( i.e. , between species of Zea , subspecies of mays , or accessions of the same species) drops by an order of magnitude for both M1 and M2 (1.31%-3.54% to 0.002-0.52%)( Figure 6 , Figure 7 ). While the percentages of exons showing more recent fractionation are small, they represent thousands of exons and hundreds of genes (M1=2,728 exons, 1,132 genes; M2=1,288 exons, 596 genes). Download figure Open in new tab Figure 6. Timing Estimates of fractionation events by exon by subgenome. The ancient WGD event is indicated by the lavender multi-pointed circle at the base of the Tripsacinae after divergence of the two outgroup species Sorghum bicolor and Anatherum virginicum . Fractionation of an exon is assigned a node based on retained status in all genomes below the node and fractionated status in all genomes above the node for a given branch. Percentage of exons that fit each pattern are labeled on the branch, colored by the corresponding subgenome (blue = M1, red = M2). Only Tripsacum and Zea mays ssp. genomes and completely aligned exons (aligned in every genome included) are used to create these estimates. Exons that do not show a monophyletic pattern are labeled “paraphyly”. Download figure Open in new tab Download figure Open in new tab Figure 7. Timing Estimates of fractionation events by exon by subgenome with a zoom in on the NAM branches, phylogeny from Hufford et. al. (2021). Labeling is the same as in Figure 6 , except only internal branches with some specific fractionation are labeled to reduce figure complexity (if a branch is unlabeled, there is no unique, monophyletic fractionation observed for that branch). Only NAM lines with tropical or temperate only ancestry are used for estimates (mixed NAM lines which are products of recent admixture between temperate and tropical populations are ignored, Mo18W, Tx303, M37W). Instances when an exon is called fractionated in a set of genomes that do not form a monophyletic clade are paraphyly. About 10% of all completely aligned exons in M1 and M2 are paraphyletic ( Figure 6 ). Thousands of combinations of genomes that could lead to paraphyly, though the most common involve only one to three genomes ( Supp. Figure 8 ). Undoubtedly, some are instances of multiple mutational origins or true paraphyly. However, given the pervasiveness of nested, polymorphic deletions, pinpointing multiple origins is currently unfeasible. Exons with paraphyletic calls may be more likely to disagree between methods using either GVCF or VCF as input files and thus may represent exons susceptible to false deletion calls, though both methods largely agree ( Supp. Figure 9 ). For these reasons, paraphyly is ignored. Of genes with exons fractionated at more recent time points of the phylogeny, only M1 genes fractionated only in Z. huehuetenagensis showed enrichment for GO terms–specifically those relating to protein-containing complexes and cellular structures– and M1 genes fractionated only in T. dactyloides KS–specifically enriched for nuclear-excision repair complex (Supplemental Data 1). M1 genes with exons that were basally fractionated (fractionated across all genomes) show enrichment for transcriptional regulation, DNA binding, and regulatory processes and depletion for terms relating to translation, protein regulation, transportation, and many cellular processes. M1 genes with exons that were basally retained (retained across all genomes) show enrichment for signaling, transport, protein modification, and metabolism. M1 genes with exons fractionated only in Tripsacum genomes were enriched for biological and cellular regulation and those fractionated only in Zea genomes were enriched for membrane and lumen binding. M2 genes with exons basally fractionated were enriched for inhibitor activity and unclassified terms and depleted for protein localization, membrane complexes, and vesicles. M2 genes with exons basally retained were enriched for protein modification and binding, transportation, metabolism, and Golgi Apparatus associated terms. M2 genes with exons fractionated only in Tripsacum genomes were enriched for positive regulation of organellar and cellular component organization and those fractionated only in Zea genomes were enriched for regulation of nuclear division and organellar organization (Supplemental Data 1). Discussion Differences in exon retention between genera may be related to separate chromosomal rearrangement histories Zea genomes retained pairs of homoeologs at similar proportions and showed similar extent of exon loss from homoeologous genes. Likewise, similar observations were made between the two Tripsacum genomes. However, there were stronger fractionation differences between genera. Tripsacum had significantly higher retention of homoeologous pairs and fewer exons lost per gene than Zea. A glaring distinction between the genera is the significant difference in chromosomal rearrangements relative to sorghum and haploid chromosome number, with Tripsacum having fewer rearrangements and 18 smaller chromosomes while Zea contains many rearrangements and 10 larger chromosomes ( Maguire 1961 ). Descending dysploidy, or a decrease in chromosome number, via translocations can occur when two non-homologous chromosomes have double stranded breaks which are resolved through nonhomologous end joining across chromosomes or non-allelic homologous recombination between repetitive sequences found on both chromosomes ( Lysák and Schubert 2013 ). Most grasses show limited descending dysploidy, with few reductions in chromosome number post-polyploidy ( Stitzer et al., 2024 , Murat et al., 2014 , Salse 2016 , Scarlett et al., 2023 ). A broader taxonomic view shows extensive chromosomal rearrangements are common after polyploidy ( Carta et al., 2020 , Li et al., 2021 , Salse 2012 ), with resynthesis experiments of Brassica napus showing chromosomal rearrangements occurring as early as the initial meiosis generation and becoming fixed after as few as 3 or 5 generations of selfing ( Szadkowski et al., 2010 ). These differences between monocots and eudicots indicate lineage specificity in chromosomal structural rearrangement post-polyploidy. Furthermore, recent studies of Microlepidieae , a crucifer tribe endemic to Australia and New Zealand, have likewise shown increased fractionation with greater numbers of chromosomal rearrangements and chromosome number reductions ( Mandáková et al., 2017b ). Changes in life history ( e.g. , transition from perennialism to annualism) could increase recombination rates, chromosomal rearrangements, and/or fractionation rates; such trends were observed, though not statistically significant, in the Microlepidieae ( Mandáková et al., 2017b ). These trends also fit with our observations of perennial Tripsacum vs. largely annual Zea species, the causal factors leading to either chromosomal rearrangement or chromosomal conservation post-polyploidy remains an open question. Fractionation status is mostly shared, but differences are driven by higher retention of Tripsacum compared to Zea Despite high levels of shared retention and fractionation across genomes, differences appear to be driven by higher retention in Tripsacum relative to Zea . However, not all differences were solely between genera. Overall, 35.2% of homoeologous exon pairs show multiple fractionation statuses, which is greater than previous reports comparing maize accessions (∼2% Brohammer et al., 2018 ; ∼6% Hufford et al., 2021 ). This would seem to indicate several non-exclusive, potentially interacting processes at play. (1) loss of an exon may be less deleterious than expected, particularly if a homoeologous exon remains intact; (2) there is selection for either retention or fractionation of a given gene or exon in a subset of lineages; (3) fractionation of an exon was not entirely fixed within ancestral populations and is continuing to segregate. It is well documented that polyploidy creates redundancy and buffers the effects of highly deleterious mutations, such as exon loss, so long as one homoeolog retains the original function ( Cheng et al., 2018 ; Zhao et al., 2017 ). Previous studies show that more highly expressed genes are more likely to be retained in maize through purifying selection ( Pophaly & Tellier, 2015 ; Renny-Byfield et al., 2017 ; Schnable et al., 2011 ). While most homoeologs of both subgenomes for which we have dN/dS estimates show signatures of purifying selection, ∼20% of exons per genome show both homoeologous exons have deletions, and > 25% of homoeologous gene pairs are fractionated under the most conservative cutoff. Subfunctionalization, where a pair of homoeologs split the original function of the gene, and neo-functionalization, where one homoeolog gains a novel function, are two other potential outcomes of polyploidy ( Bird et al., 2018 ; Cheng et al., 2018 ). If either process altered the number of exons within a given homoeolog, that could be an important source of adaptive diversity ( Cheng et al., 2018 ). The members of the Tripsacinae subtribe, while centered in the neotropics, have dispersed to environments across extreme altitude, latitude, temperature, and precipitation variation ( Brink & De Wet, 1983 ; Hufford et al., 2012 ). Given the number of privately fractionated exons for individual wild species and subspecies, neo-functionalization and sub-functionalization might have supported adaptation to these different environments, though this is difficult to prove. Finally, like any mutation, loss of an exon had to occur first in a single individual and then be passed on to subsequent generations, rising in frequency until it fixed in the lineage. However, if fractionation of an exon was polymorphic within the population during the divergence of lineages, this could result in incomplete lineage sorting (ILS). This could also explain the large numbers of exons showing differential fractionation across genomes. In order to test the extent of ILS, more individuals from each species and subspecies would need to be sequenced to detect fractionation polymorphisms. With the current data, it is difficult to determine which of these three, non-exclusive possibilities are driving the observed patterns. Sharing of gene loss likely driven by relaxed purifying selection Most genes show the exact same exons fractionated across all genomes. However, differences in exon deletion are detected that often correlate with divergence between two genomes. This suggests multiple origins of fractionation for a given homoeolog or convergence of fractionation of the same homoeolog across taxa. If multiple origins underlie fractionation of a given homoeolog, it is difficult to distinguish whether relaxed purifying selection has allowed multiple polymorphic deletions to accumulate or selection for loss of a homoeolog has led to convergent fractionation. For the subset of genes Yin et al (2022) calculated dN/dS for each subgenome of B73 and sorghum, it appears that homoeologs with more differences in which exons were lost between pairs of genomes show a higher dN/dS than those that share exon fractionation. This suggests relaxed purifying selection may be more likely the driving force behind the convergent loss of homoeologs. Timing of fractionation is early in the subtribe Given that most fractionation appears to be shared across all genomes or within genera, the majority of fractionation likely occurred either before the divergence of Tripsacum and Zea (∼5 MYA - 653 KYA, Schnable et al 2011 , Chen et al 2022 ), or after genera divergence but before Zea mays speciation and subspeciation events (∼653 KYA - 67 KYA, Chen et al 2022 ). While the majority of fractionation in M1 and M2 happened before speciation, a significant amount occurred post-speciation. This agrees with previous work that fractionation began soon after the WGD event ( Li et al., 2016 ; Sankoff et al., 2010 ; Schnable et al., 2011 ), but continued until present day, affecting thousands of genes ( Brohammer et al 2018 , Hufford et al 2021 ). There are subtle differences in the distribution of M1 and M2 fractionation across the phylogeny, which suggests that there could be differences in the rates or timing of fractionation between subgenomes. Previous work has shown that the rate of deletion mutations is similar between the subgenomes in maize ( Schnable et al., 2011 ), so it is unlikely due to different rates of mutation, but rather differences in purifying selection which could vary over time. We also assume that the number of generations is similar for each lineage, which is untrue given differences in perennial and annual life histories among taxa. Differences in effective population sizes between lineages may also affect the rate of variant, in this case deletion, fixation. Our larger sampling of maize genomes may allow detection of variable fractionation within this subspecies compared to the other wild lineages of Zea and Tripsacum . Wider genome sequencing of wild species and populations, particularly of Tripsacum , could reveal similar patterns of recent fractionation as seen in Zea mays . Assembly of Tripsacum genomes is difficult given the outcrossing heterozygous nature of most lineages, high rates of recent polyploidy, difficulty assigning species taxonomy, and difficulty extracting high molecular weight DNA from tissue ( Blakey et al., 2007 ; Brink & De Wet, 1983 ). Conclusion The larger patterns of biased subgenome fractionation occurring shortly after the polyploidy event observed from investigations in maize also hold true in this expanded study that includes wild species across the Tripsacinae . However, there are strong differences in the amount of fractionation, the way homoeologs are fractionated, and the amount of fractionation relative to the ancestral chromosomes between Zea and Tripsacum . This suggests that fractionation followed two different trajectories within the subtribe, perhaps related to the differences in chromosomal rearrangements which characterize the genera. Data Availability Statement All scripts underlying this article are available on github at https://github.com/Snodgras/Zea_Fractionation . The genome assemblies and annotations underlying this article are available at maizeGDB ( Woodhouse et al., 2021 , https://doi.org/10.1186/s12870-021-03173-5 ). Exons used for the high quality set are available in supplemental file ref_Sb313_cds.bed. Estimates of dN/dS are available in the Yin et al (2022) and in its online supplementary material. Supplemental Files Supplemental Data 1 - GO TERMS Supplemental file ref_Sb313_cds.bed - Reference Exon List Supplemental Figures Download figure Open in new tab Download figure Open in new tab Supp. Figure 1. The modern Zea chromosomes may be the product of 6 series of reciprocal translocations and chromosomal fusions between ancestral chromosomes. Two of which are in part shared with Tripsacum . These figures represent simplified hypotheses based on syntenic dot plots of how these ancestral chromosomes rearranged to become the chromosomes observed today. Chromosome colors roughly correspond to the colors used in Fig. 1 . The box outline colors correspond to ancestral subgenomes (blue = M1 and red = M2). Series A) (1) Reciprocal translocation between M1 chr 8 and M1 chr 7. (2) Reciprocal translocation between 8-7 segment and M1 chr 9 which also fissions a larger section of M1 chr 9. (3) The 7-8 segment inserts itself into M1 chr 1 resulting in the modern Zea chromosome 1. (4) The 8-7-9 segment fuses to M2 chr 6 resulting in the modern Zea chromosome 10. (5) The 7-9 segment and larger remaining segment of chr 9 fuse to M2 chr 10, resulting in the modern Zea chromosome 6. Series B) (1) Reciprocal translocation between M1 chr 10 and M2 chr 1. The 1-10 segment results in modern Zea chr 9 and modern Tripsacum chr 4. The 10-1 segment results in modern Tripsacum chromosome 10. (2) M1 chr 4 fuses to the end of the 10-1 segment resulting in modern Zea chromosome 5. Series C) (1) M2 chr 5 inserts into M2 chr 2, resulting in modern Tripsacum chromosome 5. (2) The 2-5-2 proto-chromosome fissions and recombines. (3) M1 chr 6 fuses to the end of the 5-2-5-2 proto-chromosome resulting in modern Zea chromosome 2. Series D) (1) M2 chromosome 8 inserts into M1 chromosome 3, resulting in modern Zea chromosome 3. Series E) (1) M2 chromosome 9 inserts into M2 chromosome 3, resulting in modern Zea chromosome 8. Series F) (1) Reciprocal translocation between M2 chr 7 and M1 chr 5. (2) Reciprocal translocation between the 7-5 segment and M2 chr 4. (3) Fusion of the segments from (2). (4) Fusion of the 5-7 segment from (1) to the 4-5-7-5-4 segment from (3), resulting in the modern Zea chromosome 4. Download figure Open in new tab Supp. Figure 2. Output from VCFMetrics plugin on the rate of mapping vs. alignment across genomes relative to Sorghum by sorghum reference chromosome and subgenome (M1 and M2). Mapped refers to any matches (nucleotide to nucleotide or gap) while aligned refers to exact matches (nucleotide to nucleotide). Thus, mapping rates were high, while alignment rates were low due to large amounts of deletion in Tripsacinae genomes relative to Sorghum. Dark triangles indicate 4 to 1 mapping of genomes rather than 2 to 1 mapping, while the red triangle differentiates Td KS (triangle) from Td FL (open circle). Download figure Open in new tab Supp. Figure 3. Percentage of reference exons identified as aligned and either completely retained (“Retained”) or some loss (“Deleted”) or as “Unaligned” across subgenomes M1 and M2 for all Tripsacinae genomes. Download figure Open in new tab Download figure Open in new tab Supp. Figure 4. Percent gene lost by genome and subgenome (top) and average percent gene lost by subgenome (bottom). Percentages calculated from number of exons called fractionated out of the total number of exons within the reference gene annotation. Download figure Open in new tab Supp. Figure 5. Number of ways a homoeolog was lost. Violin plot shows the distribution of homoeologs by subgenome that show different patterns of loss, starting at 1 loss pattern. Loss patterns are defined as the combination of exons called fractionated within the gene model. Download figure Open in new tab Download figure Open in new tab Download figure Open in new tab Supp. Figure 6. Heatmap showing the percentage of genes between any pair-wise comparison of genomes that show different levels of fractionation sharing. Empty tiles correspond to no observations of that category between those two genomes. Brighter colors indicate more genes. Download figure Open in new tab Download figure Open in new tab Supp. Figure 7. Average dN/dS from ( Yin et al 2022 ) for different convergence categories where both genomes show some fractionation. Split by M1 (top) and M2 (bottom) homoeologs. Brighter colors mean higher dN/dS. Empty cells mean there were no genes observed in that comparison in that category. Download figure Open in new tab Supp. Figure 8. Frequency of paraphyly patterns by the number of genomes involved. Each paraphyly pattern is created by a unique, paraphyletic relationship involving at least 2 genomes and no more than 34 ( Z. nicaraguensis excluded). The number of exons displaying a given paraphyletic pattern is along the y-axis and the number of genomes involved in that pattern are on the x-axis. Download figure Open in new tab Supp. Figure 9. Agreement between GVCF and VCF input file fractionation calls. Different categories refer to the different calls made by methods using either GVCF or VCF files as the starting point. “Ret.” means “Retained”. Tiles represent possible combinations of calls for a pair of homoeologous exons under the two methods. Colors refer to percent of all exon pairs with lighter colors meaning more exons. Acknowledgements We would like to acknowledge our funding sources: DGE#1744592, NSF-IOS 1822330, and NSF-IOS 2305694, MRI1726447, and MRI2018594, which supported the sequencing, computational, and labor costs of this project. We thank the practical haplotype graph team, especially Ana Helene Berthel and Zach Miller, who generously helped troubleshoot the MAF to GVCF plugin in Tassel5. We thank Jonathan Wendel for his advice on this project and general enthusiasm and encouragement in all things polyploid. We thank Elli Cryan for her insights on dN/dS pipelines. This research was also supported by the US. Department of Agriculture, Agricultural Research Service, Project Number [5030-21000-072-00-D] through the Corn Insects and Crop Genetics Research Unit in Ames, Iowa. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and Employer. Footnotes https://github.com/Snodgras/Zea_Fractionation https://doi.org/10.1186/s12870-021-03173-5 https://doi.org/10.1093/molbev/msac198 References ↵ Anderson , Edgar . ( 1944 ). Cytological Observations on Tripsacum dactyloides . Annals of the Missouri Botanical Garden , 31 ( 4 ): 317 . doi: 10.2307/2394366 OpenUrl CrossRef Barker , M. 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