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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
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    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.
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