Chromosome-scale assembly of the genome of<i>Salix dunnii</i>reveals a male-heterogametic sex determination system on chromosome 7

He, Li; Jia, Kai‐Hua; Zhang, Rengang; Wang, Yuan; Shi, Tian-Le; Li, Zhichao; Zeng, Si-Wen; Cai, Xin-Jie; Wagner, Natascha; Hoerandl, Elvira; Muyle, Aline; Yang, Ke; Charlesworth, Deborah; Mao, Jian‐Feng

doi:10.1101/2020.10.09.333229

Cited by 8 publications

(11 citation statements)

References 119 publications

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“…A recent study analyzed differences in sex determination systems in subg. Salix and the Chamaetia/Vetrix clade, which might be responsible for incompatibilities between the two subgeneric clades (He et al, 2021a). This would support our conclusion that the plastomes of the subgenera evolved more independently.…”

Section: Molecular Dating Opposed Hypotheses Of Rapid Radiation or Rapid Range Expansion From Refugiasupporting

confidence: 83%

Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes

2021

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Plastome phylogenomics is used in a broad range of studies where single markers do not bear enough information. Phylogenetic reconstruction in the genus Salix is difficult due to the lack of informative characters and reticulate evolution. Here, we use a genome skimming approach to reconstruct 41 complete plastomes of 32 Eurasian and North American Salix species representing different lineages, different ploidy levels, and separate geographic regions. We combined our plastomes with published data from Genbank to build a comprehensive phylogeny of 61 samples (50 species) using RAxML (Randomized Axelerated Maximum Likelihood). Additionally, haplotype networks for two observed subclades were calculated, and 72 genes were tested to be under selection. The results revealed a highly conserved structure of the observed plastomes. Within the genus, we observed a variation of 1.68%, most of which separated subg. Salix from the subgeneric Chamaetia/Vetrix clade. Our data generally confirm previous plastid phylogenies, however, within Chamaetia/Vetrix phylogenetic results represented neither taxonomical classifications nor geographical regions. Non-coding DNA regions were responsible for most of the observed variation within subclades and 5.6% of the analyzed genes showed signals of diversifying selection. A comparison of nuclear restriction site associated DNA (RAD) sequencing and plastome data on a subset of 10 species showed discrepancies in topology and resolution. We assume that a combination of (i) a very low mutation rate due to efficient mechanisms preventing mutagenesis, (ii) reticulate evolution, including ancient and ongoing hybridization, and (iii) homoplasy has shaped plastome evolution in willows.

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Section: Molecular Dating Opposed Hypotheses Of Rapid Radiation or Rapid Range Expansion From Refugiasupporting

confidence: 83%

Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes

2021

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“…In this study, we identified and assembled the SDRs of two additional Salix species. Salix chaenomeloides has an XY SDR on chr7, which is in a similar location as a previously described SDR in S. nigra [29] and S. dunnii [52]. All three of these species are in subgenus Protitea [57].…”

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confidence: 83%

“…In contrast, sex determination regions (SDRs) were previously identified on chr15 with a ZW system in multiple willow species of subgenus Vetrix (including S. purpurea, S. viminalis and S. suchowensis) [54,55,57,58] and S. triandra of subgenus Salix [59], until the recent identification of the XY system on chr7 of two willow species from subgenus Protitea (S. nigra and S. dunnii) (Fig. 1A) [29,52].…”

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confidence: 98%

“…Populus (poplars) and Salix (willows; Salicaceae) are sister genera that are almost entirely dioecious [48][49][50][51], and their high diversity of homomorphic XY and ZW sex chromosomes [4,25,27,29,[52][53][54][55][56][57] is ideal for studying the evolutionary forces driving sex chromosome turnover in plants. Recent studies have shown a wide range of diversity and structural complexity in the sex determination systems of Salicaceae species, especially in poplars where both XY systems on chromosome (chr) 14 and 19, and a ZW system on chr19 have been reported [4,25,27,30,53,56].…”

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confidence: 99%

“…Solid lines represent the mapping depth across these regions and dotted lines represent the genome-wide average depth (S. purpurea and S. viminalis), intact RR genes have also been detected in the W-SDRs of chr15 [54,57], which suggests that Salix may have the same sex determination mechanism as Populus. Because the non-recombining SDRs are large (approximately 2-7.4 Mb with 111-488 genes) in willows, they offer the opportunity to test among evolutionary forces that drive their sex chromosome turnover [29,52,54,57], in contrast to the short SDRs (approximately 33-658 kb) with fewer protein-coding genes (4-37) usually found in poplars [4,25,27,53,56]. Although the poplar SDRs are generally smaller, there is no indication that specific SDRs are younger than in willows, as they are shared across a wide taxonomic breadth including both Asian and North American species [53,56,60].…”

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confidence: 99%

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Repeated turnovers keep sex chromosomes young in willows

Wang

et al. 2022

Genome Biol

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Background Salicaceae species have diverse sex determination systems and frequent sex chromosome turnovers. However, compared with poplars, the diversity of sex determination in willows is poorly understood, and little is known about the evolutionary forces driving their turnover. Here, we characterized the sex determination in two Salix species, S. chaenomeloides and S. arbutifolia, which have an XY system on chromosome 7 and 15, respectively. Results Based on the assemblies of their sex determination regions, we found that the sex determination mechanism of willows may have underlying similarities with poplars, both involving intact and/or partial homologs of a type A cytokinin response regulator (RR) gene. Comparative analyses suggested that at least two sex turnover events have occurred in Salix, one preserving the ancestral pattern of male heterogamety, and the other changing heterogametic sex from XY to ZW, which could be partly explained by the “deleterious mutation load” and “sexually antagonistic selection” theoretical models. We hypothesize that these repeated turnovers keep sex chromosomes of willow species in a perpetually young state, leading to limited degeneration. Conclusions Our findings further improve the evolutionary trajectory of sex chromosomes in Salicaceae species, explore the evolutionary forces driving the repeated turnovers of their sex chromosomes, and provide a valuable reference for the study of sex chromosomes in other species.

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Evolution of the spinach sex-linked region within a rarely recombining pericentromeric region

She

Liu

et al. 2023

Plant Physiology

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Sex chromosomes have evolved independently in many different plant lineages. Here, we describe reference genomes for spinach (Spinacia oleracea) X and Y haplotypes by sequencing homozygous XX females and YY males. The long arm of the 185 Mb chromosome 4 carries a 13 Mb X-linked region (XLR) and 24.1 Mb Y-linked region (YLR), of which 10 Mb is Y-specific. We describe evidence that this reflects insertions of autosomal sequences creating a “Y duplication region” or “YDR” whose presence probably directly reduces genetic recombination in the immediately flanking regions, although both the X and Y Sex-Linked Regions are within a large pericentromeric region of chromosome 4 that recombines rarely in meiosis of both sexes. Sequence divergence estimates using synonymous sites indicate that YDR genes started diverging from their likely autosomal progenitors about 3 MYA, around the time when the flanking YLR stopped recombining with the XLR. These flanking regions have a higher density of repetitive sequences in the YY than the XX assembly and include slightly more pseudogenes compared with the XLR, and the YLR has lost about 11% of the ancestral genes, suggesting some degeneration. Insertion of a male-determining factor would have caused Y-linkage across the entire pericentromeric region, creating physically small, highly recombining, terminal pseudo-autosomal regions. These findings provide a broader understanding of the origin of sex chromosomes in spinach.

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Chromosome-scale assembly of the genome ofSalix dunniireveals a male-heterogametic sex determination system on chromosome 7

Cited by 8 publications

References 119 publications

Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes

Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes

Repeated turnovers keep sex chromosomes young in willows

Evolution of the spinach sex-linked region within a rarely recombining pericentromeric region

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