IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51158-3.html
   My bibliography  Save this article

Allopolyploidization from two dioecious ancestors leads to recurrent evolution of sex chromosomes

Author

Listed:
  • Li He

    (Shanghai Chenshan Botanical Garden)

  • Yuàn Wang

    (Shanghai Chenshan Botanical Garden)

  • Yi Wang

    (Shanghai Chenshan Botanical Garden
    School of Ecology and Nature Conservation, Beijing Forestry University)

  • Ren-Gang Zhang

    (Kunming Institute of Botany, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yuán Wang

    (Shanghai Chenshan Botanical Garden)

  • Elvira Hörandl

    (Biodiversity and Evolution of Plants (with Herbarium), University of Göttingen)

  • Tao Ma

    (College of Life Science, Sichuan University)

  • Yan-Fei Mao

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences)

  • Judith E. Mank

    (University of British Columbia)

  • Ray Ming

    (Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University)

Abstract

Polyploidization presents an unusual challenge for species with sex chromosomes, as it can lead to complex combinations of sex chromosomes that disrupt reproductive development. This is particularly true for allopolyploidization between species with different sex chromosome systems. Here, we assemble haplotype-resolved chromosome-level genomes of a female allotetraploid weeping willow (Salix babylonica) and a male diploid S. dunnii. We show that weeping willow arose from crosses between a female ancestor from the Salix-clade, which has XY sex chromosomes on chromosome 7, and a male ancestor from the Vetrix-clade, which has ancestral XY sex chromosomes on chromosome 15. We find that weeping willow has one pair of sex chromosomes, ZW on chromosome 15, that derived from the ancestral XY sex chromosomes in the male ancestor of the Vetrix-clade. Moreover, the ancestral 7X chromosomes from the female ancestor of the Salix-clade have reverted to autosomal inheritance. Duplicated intact ARR17-like genes on the four homologous chromosomes 19 likely have contributed to the maintenance of dioecy during polyploidization and sex chromosome turnover. Taken together, our results suggest the rapid evolution and reversion of sex chromosomes following allopolyploidization in weeping willow.

Suggested Citation

  • Li He & Yuàn Wang & Yi Wang & Ren-Gang Zhang & Yuán Wang & Elvira Hörandl & Tao Ma & Yan-Fei Mao & Judith E. Mank & Ray Ming, 2024. "Allopolyploidization from two dioecious ancestors leads to recurrent evolution of sex chromosomes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51158-3
    DOI: 10.1038/s41467-024-51158-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51158-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51158-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Killick, Rebecca & Eckley, Idris A., 2014. "changepoint: An R Package for Changepoint Analysis," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 58(i03).
    2. Alison E. Wright & Rebecca Dean & Fabian Zimmer & Judith E. Mank, 2016. "How to make a sex chromosome," Nature Communications, Nature, vol. 7(1), pages 1-8, November.
    3. Peng Xu & Jian Xu & Guangjian Liu & Lin Chen & Zhixiong Zhou & Wenzhu Peng & Yanliang Jiang & Zixia Zhao & Zhiying Jia & Yonghua Sun & Yidi Wu & Baohua Chen & Fei Pu & Jianxin Feng & Jing Luo & Jing C, 2019. "The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Petter Arnesen & Odd A. Hjelkrem, 2018. "An Estimator for Traffic Breakdown Probability Based on Classification of Transitional Breakdown Events," Transportation Science, INFORMS, vol. 52(3), pages 593-602, June.
    2. Dehler-Holland, Joris & Schumacher, Kira & Fichtner, Wolf, 2021. "Topic Modeling Uncovers Shifts in Media Framing of the German Renewable Energy Act," EconStor Open Access Articles and Book Chapters, ZBW - Leibniz Information Centre for Economics, vol. 2(1).
    3. Malte Willmes & Katherine M Ransom & Levi S Lewis & Christian T Denney & Justin J G Glessner & James A Hobbs, 2018. "IsoFishR: An application for reproducible data reduction and analysis of strontium isotope ratios (87Sr/86Sr) obtained via laser-ablation MC-ICP-MS," PLOS ONE, Public Library of Science, vol. 13(9), pages 1-15, September.
    4. Salvatore Fasola & Vito M. R. Muggeo & Helmut Küchenhoff, 2018. "A heuristic, iterative algorithm for change-point detection in abrupt change models," Computational Statistics, Springer, vol. 33(2), pages 997-1015, June.
    5. Tasadduq Imam, 2021. "Model selection for one‐day‐ahead AUD/USD, AUD/EUR forecasts," International Journal of Finance & Economics, John Wiley & Sons, Ltd., vol. 26(2), pages 1808-1824, April.
    6. Raputsoane, Leroi, 2018. "Temporal homogeneity between financial stress and the economic cycle," MPRA Paper 91119, University Library of Munich, Germany.
    7. Hui Zhang & Minna Väliranta & Graeme T. Swindles & Marco A. Aquino-López & Donal Mullan & Ning Tan & Matthew Amesbury & Kirill V. Babeshko & Kunshan Bao & Anatoly Bobrov & Viktor Chernyshov & Marissa , 2022. "Recent climate change has driven divergent hydrological shifts in high-latitude peatlands," Nature Communications, Nature, vol. 13(1), pages 1-7, December.
    8. Subhashis Chatterjee & Ankur Shukla, 2016. "Change point–based software reliability model under imperfect debugging with revised concept of fault dependency," Journal of Risk and Reliability, , vol. 230(6), pages 579-597, December.
    9. Josephine R. Paris & James R. Whiting & Mitchel J. Daniel & Joan Ferrer Obiol & Paul J. Parsons & Mijke J. Zee & Christopher W. Wheat & Kimberly A. Hughes & Bonnie A. Fraser, 2022. "A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Joni Virta & Niko Lietzén & Henri Nyberg, 2024. "Robust signal dimension estimation via SURE," Statistical Papers, Springer, vol. 65(5), pages 3007-3038, July.
    11. C Jara-Figueroa & Amy Z Yu & César A Hidalgo, 2019. "How the medium shapes the message: Printing and the rise of the arts and sciences," PLOS ONE, Public Library of Science, vol. 14(2), pages 1-14, February.
    12. Dehler-Holland, Joris & Okoh, Marvin & Keles, Dogan, 2022. "Assessing technology legitimacy with topic models and sentiment analysis – The case of wind power in Germany," Technological Forecasting and Social Change, Elsevier, vol. 175(C).
    13. Manfren, Massimiliano & Nastasi, Benedetto, 2023. "Interpretable data-driven building load profiles modelling for Measurement and Verification 2.0," Energy, Elsevier, vol. 283(C).
    14. Rafaï, Ismaël & Blayac, Thierry & Dubois, Dimitri & Duchêne, Sébastien & Nguyen-Van, Phu & Ventelou, Bruno & Willinger, Marc, 2023. "Stated preferences outperform elicited preferences for predicting reported compliance with COVID-19 prophylactic measures," Journal of Behavioral and Experimental Economics (formerly The Journal of Socio-Economics), Elsevier, vol. 107(C).
    15. Heiner Kuhl & Kang Du & Manfred Schartl & Lukáš Kalous & Matthias Stöck & Dunja K. Lamatsch, 2022. "Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Tiago Tamagusko & Adelino Ferreira, 2020. "Data-Driven Approach to Understand the Mobility Patterns of the Portuguese Population during the COVID-19 Pandemic," Sustainability, MDPI, vol. 12(22), pages 1-12, November.
    17. Li, Boyan & Diao, Xundi, 2023. "Structural break in different stock index markets in China," The North American Journal of Economics and Finance, Elsevier, vol. 65(C).
    18. Beytía, Pablo & Infante, Carlos Cruz, 2020. "Digital Pathways, Pandemic Trajectories. Using Google Trends to Track Social Responses to COVID-19," SocArXiv yndb7, Center for Open Science.
    19. Kuebart, Andreas & Stabler, Martin, 2023. "Waves in time, but not in space – an analysis of pandemic severity of COVID-19 in Germany," EconStor Open Access Articles and Book Chapters, ZBW - Leibniz Information Centre for Economics, vol. 47.
    20. Subhashis Chatterjee & Ankur Shukla, 2017. "An Ideal Software Release Policy for an Improved Software Reliability Growth Model Incorporating Imperfect Debugging with Fault Removal Efficiency and Change Point," Asia-Pacific Journal of Operational Research (APJOR), World Scientific Publishing Co. Pte. Ltd., vol. 34(03), pages 1-21, June.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51158-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.