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The male-heterogametic sex determination system on chromosome 15 of Salix triandra and Salix arbutifolia reveals ancestral male heterogamety and subsequent turnover events in the genus Salix

A Correction to this article was published on 31 January 2023

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Abstract

Dioecious Salix evolved more than 45 million years ago, but have homomorphic sex chromosomes, suggesting that turnover event(s) prevented major differentiation. Sex chromosome turnover events have been inferred in the sister genus Populus. The genus Salix includes two main clades, Salix and Vetrix, with several previously studied Vetrix clade species having female-heterogametic (ZW) or male-heterogametic (XY) sex-determining systems (SDSs) on chromosome 15, while three Salix clade species have XY SDSs on chromosome 7. We here studied two basal taxa of the Vetrix clade, S. arbutifolia and S. triandra using S. purpurea as the reference genome. Analyses of whole genome resequencing data for genome-wide associations (GWAS) with the sexes and genetic differentiation between the sexes (FST values) showed that both species have male heterogamety with a sex-determining locus on chromosome 15, suggesting an early turnover event within the Vetrix clade, perhaps promoted by sexually antagonistic or (and) sex-ratio selection. Changepoint analysis based on FST values identified small sex-linked regions of ~3.33 Mb and ~2.80 Mb in S. arbutifolia and S. triandra, respectively. The SDS of S. arbutifolia was consistent with recent results that used its own genome as reference. Ancestral state reconstruction of SDS suggests that at least two turnover events occurred in Salix.

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Fig. 1: Phylogenetic tree of willow species with known sex systems and the outgroup Populus euphratica.
Fig. 2: Identification of the sex determination system of Salix triandra.
Fig. 3: Identification of the sex determination system of Salix arbutifolia.
Fig. 4: Reconstructions of ancestral sex determination system and character of willow species.

Data availability

Sequence data presented in this article can be downloaded from the National Center for Biotechnology Information Sequence Read Archive (NCBI SRA) under the BioProject accession number PRJNA882493.

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Acknowledgements

We thank Deborah Charlesworth for her useful comments on our paper. We thank Zhenfeng Zhan of Beijing Forestry University and Xiaobai Shang for assistance with the samples collection.

Funding

This study was financially supported by the National Natural Science Foundation of China (grant No. 32171813).

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YW, EH, LH and ZZ planned and designed the research. YW, LH and XC analysed the data. YZ collected samples. All authors have read, commented and approved the manuscript.

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Correspondence to Zhixiang Zhang or Li He.

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Wang, Y., Cai, X., Zhang, Y. et al. The male-heterogametic sex determination system on chromosome 15 of Salix triandra and Salix arbutifolia reveals ancestral male heterogamety and subsequent turnover events in the genus Salix. Heredity 130, 122–134 (2023). https://doi.org/10.1038/s41437-022-00586-2

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