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

Li He (), Yuàn Wang, Yi Wang, Ren-Gang Zhang, Yuán Wang, Elvira Hörandl, Tao Ma, Yan-Fei Mao, Judith E. Mank and Ray Ming
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Li He: Shanghai Chenshan Botanical Garden
Yuàn Wang: Shanghai Chenshan Botanical Garden
Yi Wang: Shanghai Chenshan Botanical Garden
Ren-Gang Zhang: Kunming Institute of Botany, 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

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-51158-3

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