Haplotype-resolved genome assembly of a male Dioscorea alata cultivar reveals the structure and evolution of sex chromosomes

Haplotype-resolved genome assembly of a male Dioscorea alata cultivar reveals the structure and evolution of sex chromosomes | 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 Haplotype-resolved genome assembly of a male Dioscorea alata cultivar reveals the structure and evolution of sex chromosomes Komivi Dossa, Xiaojun Su, Yedomon Ange Bovys Zoclanclounon, Yao Chen, and 18 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5627324/v2 This work is licensed under a CC BY 4.0 License Status: Posted Version 2 posted You are reading this latest preprint version Show more versions Abstract Dioscorea alata L., the most widely cultivated yam species, exhibits dioecy (XY system) and a strong male-biased sex ratio. These two major constraints limit parental combinations and hinder breeding progress. To get insight into the sex chromosome structure and evolution in D. alata , we present a haplotype-resolved, near-complete genome assembly of the male cultivar ‘Kabusa’, spanning 958 Mb across 40 chromosomes. DalaChr6A is identified as the Y chromosome which exhibits early signs of heteromorphism, including a slight reduction in size (∼400 Kb difference) and a potential centromere shift relative to the X chromosome. Our findings also reveal a sex chromosome turnover between D. alata and D. rotundata . The sex chromosomes of D. alata are evolutionarily young (~4.32 million year ago) and emerged after the divergence from the D. rotundata lineage. The sex-determining region (SDR) is refined to ∼7.6 Mb, representing ~44% of the Y chromosome. It contains several inversions and a divergence gradient was observed across these inversions. INV4 identified as the oldest pericentric inversion likely marks the early step in D. alata SDR evolution. Despite structural divergence, both X and Y chromosomes remain transcriptionally active. Among the 231 genes annotated in the SDR, 97 are sex-biased and enriched in functions associated with floral organ formation and hormonal signaling pathways. This study enhances our understanding of sex chromosome evolution and sex determination in dioecious plants. It provides a gold-standard reference genome for the Dioscorea genus and lays the foundation for accelerated breeding and genetic improvement in yam. dioecy root and tuber crops structural variants genetic gain genome Figures Figure 1 Figure 2 Figure 3 Figure 4 Full Text Additional Declarations The authors declare no competing interests. Supplementary Files SupplementaryTables.xlsx SupplementaryFigures.pdf Cite Share Download PDF Status: Posted Version 2 posted You are reading this latest preprint version Show more versions 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-5627324","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":401961813,"identity":"f9a730ae-e61c-4199-8580-451071148ed5","order_by":0,"name":"Komivi 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(\u003cstrong\u003ea\u003c/strong\u003e) Pictures of ‘Kabusa’ cultivar displaying the aerial biomass in the field, the tuber shape and flesh color, and the male flowers. (\u003cstrong\u003eb\u003c/strong\u003e) Genome-wide Hi-C contact heatmap, visualized with Juicebox\u003csup\u003e32\u003c/sup\u003e. (\u003cstrong\u003ec\u003c/strong\u003e) Circle diagram of basic genome information. Concentric circles from outside to inside represent chromosomes, gene density, repeat density, and GC density calculated in a 50 Kb window. Lines in the interior indicate collinearity. The scale bar = 10 cm. (\u003cstrong\u003ed\u003c/strong\u003e) Syntenic mapping between the two haplotypes of the ‘Kabusa’ genome using SyRI\u003csup\u003e33\u003c/sup\u003e. Collinear regions between HaplotypeA and HaplotypeB are indicated with gray lines, while inversion, translocation, and duplication regions are indicated with orange, green, and blue lines, respectively.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/944e4ad07abd6f12e727c028.png"},{"id":90921508,"identity":"4be49b5e-9194-4a9e-9a7c-f3e6f09adfbe","added_by":"auto","created_at":"2025-09-09 14:54:29","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":1589746,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eStructure of the sex determination region (SDR) in \u003c/strong\u003e\u003cem\u003e\u003cstrong\u003eD. alata\u003c/strong\u003e\u003c/em\u003e\u003cstrong\u003e. \u003c/strong\u003e(\u003cstrong\u003ea\u003c/strong\u003e)\u003cstrong\u003e \u003c/strong\u003eHi-C contact heatmap between\u003cstrong\u003e \u003c/strong\u003eDalaChr6A (Y) and DalaChr6B (X), visualized with Juicebox [\u003ca href=\"#_ENREF_31\" title=\"Durand, 2016 #32\"\u003e31\u003c/a\u003e]. (\u003cstrong\u003eb\u003c/strong\u003e) Syntenic mapping between ‘Kabusa’ Y chromosome and X chromosomes from ‘Kabusa’, Dala_V2\u003csup\u003e27\u003c/sup\u003e and Ziyushenshu\u003csup\u003e28\u003c/sup\u003e using SyRI\u003csup\u003e33\u003c/sup\u003e. Four inversions (INV1-INV4) were detected. (\u003cstrong\u003ec\u003c/strong\u003e) The genomic landscape of genetic variants between male and female pools. The outer track represents the 20 chromosomes (chr) of HaplotypeA in the ‘Kabusa’ genome. The inner tracks from outside to inside represent \u003cem\u003eFst\u003c/em\u003e between females and males and male-specific SNP density, respectively (window size 100 Kb). (\u003cstrong\u003ed\u003c/strong\u003e) Manhattan plot for SNP-sex phenotype genome-wide association study (GWAS), with the peaks indicating significant GWAS signals, and the black and red dotted horizontal lines indicating the suggestive and genome-wide significance thresholds, respectively. (\u003cstrong\u003ee\u003c/strong\u003e) Manhattan plot for InDel-sex phenotype GWAS, with the peaks indicating significant GWAS signals, and the black and red dotted horizontal lines indicating the suggestive and genome-wide significance thresholds, respectively. Regional Manhattan plots on DalaChr6A showing the dispersion of the significant SNPs (\u003cstrong\u003ef\u003c/strong\u003e) and Indels (\u003cstrong\u003eg\u003c/strong\u003e). (\u003cstrong\u003eh\u003c/strong\u003e) Differential read coverage (10 Kb window) between male and female groups along the Y chromosome. (\u003cstrong\u003ei\u003c/strong\u003e) Exact matches of male specific 27-mers along the Y chromosome. (\u003cstrong\u003ej\u003c/strong\u003e) Representation of the X (DalaChr6B) and Y (DalaChr6A) chromosomes along with the gene density (heatmap), centromere and telomere locations, pseudoautosomal regions (PAR), and the SDR containing the 4 inversions (INV1-INV4) detected.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/547cf9794f0aff43f4777378.png"},{"id":90921511,"identity":"d3f1d3d3-61da-47b7-a04b-7897268a6a53","added_by":"auto","created_at":"2025-09-09 14:54:29","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":546618,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eSex chromosome divergence in \u003c/strong\u003e\u003cem\u003e\u003cstrong\u003eD. alata\u003c/strong\u003e\u003c/em\u003e\u003cem\u003e. \u003c/em\u003e(\u003cstrong\u003ea\u003c/strong\u003e) Comparison of the synonymous substitution rates (\u003cem\u003eKs\u003c/em\u003e) of genes between SDR and PAR on the Y chromosome. (\u003cstrong\u003eb\u003c/strong\u003e) \u003cem\u003eKs\u003c/em\u003e comparison between Y chromosome components. ** = significant difference at \u003cem\u003ep\u003c/em\u003e \u0026lt;0.001. (\u003cstrong\u003ec\u003c/strong\u003e) Comparison of the LTR/Copia and LTR/Gypsy densities between PAR and SDR in the Y chromosome. (\u003cstrong\u003ed\u003c/strong\u003e) Comparison of the LTR/Copia and LTR/Gypsy densities between PAR and HXR in the X chromosome. (\u003cstrong\u003ee\u003c/strong\u003e) Comparison of the LTR/Copia and LTR/Gypsy densities between SDR and HXR. (\u003cstrong\u003ef\u003c/strong\u003e) Smoothed density plots along X and Y chromosomes. Densities are calculated per 1 Mb overlapping windows.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/e49d9bde17a5db01af30dc41.png"},{"id":90921512,"identity":"31041e48-18b1-4e4f-88f3-1493c4c8f4c2","added_by":"auto","created_at":"2025-09-09 14:54:29","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":607634,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eSex-biased gene expression in \u003c/strong\u003e\u003cem\u003e\u003cstrong\u003eD. alata\u003c/strong\u003e\u003c/em\u003e\u003cstrong\u003e. \u003c/strong\u003e(\u003cstrong\u003ea\u003c/strong\u003e) Development of \u003cem\u003eD. alata\u003c/em\u003e flower at Day5, Day8 and Day12 after blooming in male ‘Kabusa’ and female ‘74F’. Ontogenetic differences between female and male flowers become morphologically evident between Day8 and Day12 after blooming. Scale = 1 cm. (\u003cstrong\u003eb\u003c/strong\u003e) Principal component analysis based on the gene expression levels for flower samples (Day5) expressed as fragments per kilobase of transcript per million fragments mapped in the male and female groups. The first and the second principal components explaining 55% and 20% of the total variation, respectively. (\u003cstrong\u003ec\u003c/strong\u003e) Volcano plot displaying the differential expression analysis in flowers between male and female groups. Dots in green, red, and gray represent genes downregulated, upregulated and not differentially expressed in male flowers compared to female flowers, respectively. (\u003cstrong\u003ed\u003c/strong\u003e) Gene expression patterns in flower buds (log\u003csub\u003e2\u003c/sub\u003efold change between male and female groups) along the sex chromosomes. Each dot represents a sex-biased gene (SBG). Statistical comparison of SBG located within the sex chromosomes (\u003cstrong\u003ee\u003c/strong\u003e) and within the Y chromosome components (\u003cstrong\u003ef\u003c/strong\u003e). (\u003cstrong\u003eg\u003c/strong\u003e) Statistical comparison of SGB in mature tuber samples located within the sex chromosomes. Samples represent mature tuber from three female \u003cem\u003eD. alata\u003c/em\u003e accessions (‘Dou’, ‘Kinabayo’, and ‘74F’) and three male accessions (‘Divin’, ‘Plimbite’, and ‘Toufi-Tetea’). * = significant difference at \u003cem\u003ep\u003c/em\u003e \u0026lt;0.05. (\u003cstrong\u003eh\u003c/strong\u003e) Comparison of the methylation levels (5-methylcytosine at CpG sites) across sex chromosomes and statistical comparison between sex chromosomes components: SDR vs PAR (\u003cstrong\u003ei\u003c/strong\u003e), HXR vs PAR (\u003cstrong\u003ej\u003c/strong\u003e) and SDR vs HXR (\u003cstrong\u003ek\u003c/strong\u003e). Methylation levels are calculated per 100 Kb overlapping windows.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/87edcae692862b2039fe015d.png"},{"id":90925478,"identity":"c0bfdd9b-4ee8-4068-80c4-580d3004c510","added_by":"auto","created_at":"2025-09-09 15:26:34","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1574065,"visible":true,"origin":"","legend":"","description":"","filename":"Kabusagenomedraft.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2_covered_1149b082-32a8-4dca-993f-e283753527bd.pdf"},{"id":90921509,"identity":"e1acdda2-ce29-4637-ad66-88782cdefb8f","added_by":"auto","created_at":"2025-09-09 14:54:29","extension":"xlsx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":293723,"visible":true,"origin":"","legend":"","description":"","filename":"SupplementaryTables.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/206dad528dc8fb4121faab6a.xlsx"},{"id":90921515,"identity":"eff0a657-55de-448e-be5c-b1aa32481edf","added_by":"auto","created_at":"2025-09-09 14:54:29","extension":"pdf","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":11308238,"visible":true,"origin":"","legend":"","description":"","filename":"SupplementaryFigures.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5627324/v2/8bab078b4707e842128a3ba7.pdf"}],"financialInterests":"The authors declare no competing interests.","formattedTitle":"\u003cp\u003e\u003cstrong\u003eHaplotype-resolved genome assembly of a male \u003c/strong\u003e\u003cem\u003e\u003cstrong\u003eDioscorea alata\u003c/strong\u003e\u003c/em\u003e\u003cstrong\u003e cultivar reveals the structure and evolution of sex chromosomes\u003c/strong\u003e\u003c/p\u003e","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"dioecy, root and tuber crops, structural variants, genetic gain, genome","lastPublishedDoi":"10.21203/rs.3.rs-5627324/v2","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5627324/v2","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cem\u003eDioscorea alata \u003c/em\u003eL., the most widely cultivated yam species, exhibits dioecy (XY system) and a strong male-biased sex ratio. These two major constraints limit parental combinations and hinder breeding progress. To get insight into the sex chromosome structure and evolution in \u003cem\u003eD. alata\u003c/em\u003e, we present a haplotype-resolved, near-complete genome assembly of the male cultivar ‘Kabusa’, spanning 958 Mb across 40 chromosomes. DalaChr6A is identified as the Y chromosome which exhibits early signs of heteromorphism, including a slight reduction in size (∼400 Kb difference) and a potential centromere shift relative to the X chromosome. Our findings also reveal a sex chromosome turnover between \u003cem\u003eD. alata\u003c/em\u003e and \u003cem\u003eD. rotundata\u003c/em\u003e. The sex chromosomes of \u003cem\u003eD. alata\u003c/em\u003e are evolutionarily young (~4.32 million year ago) and emerged after the divergence from the \u003cem\u003eD. rotundata\u003c/em\u003e lineage. The sex-determining region (SDR) is refined to ∼7.6 Mb, representing ~44% of the Y chromosome. It contains several inversions and a divergence gradient was observed across these inversions. INV4 identified as the oldest pericentric inversion likely marks the early step in \u003cem\u003eD. alata\u003c/em\u003e SDR evolution. Despite structural divergence, both X and Y chromosomes remain transcriptionally active. Among the 231 genes annotated in the SDR, 97 are sex-biased and enriched in functions associated with floral organ formation and hormonal signaling pathways. This study enhances our understanding of sex chromosome evolution and sex determination in dioecious plants. It provides a gold-standard reference genome for the \u003cem\u003eDioscorea\u003c/em\u003e genus and lays the foundation for accelerated breeding and genetic improvement in yam.\u003c/p\u003e","manuscriptTitle":"Haplotype-resolved genome assembly of a male Dioscorea alata cultivar reveals the structure and evolution of sex chromosomes","msid":"","msnumber":"","nonDraftVersions":[{"code":2,"date":"2025-09-09 14:54:24","doi":"10.21203/rs.3.rs-5627324/v2","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}},{"code":1,"date":"2025-01-14 10:43:59","doi":"10.21203/rs.3.rs-5627324/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"26af1965-693c-4923-901c-20dad109ce47","owner":[],"postedDate":"September 9th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2025-01-14T10:52:02+00:00","versionOfRecord":[],"versionCreatedAt":"2025-09-09 14:54:24","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v2","identity":"rs-5627324","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5627324","identity":"rs-5627324","version":["v2"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}