Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

Abstract

Background: Sex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes, and this leads to a range of non-adaptive modifications causing gradual degeneration and gene loss on the sex-limited chromosome. However, the proximal causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear. Results: Here, we use long-and short-read single-molecule sequencing approaches to assemble and annotate a draft genome of the basket willow, Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W single-nucleotide divergence in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although the W-linked region contains genes involved in cytokinin signaling regulation that are not syntenic with the Z homolog. Furthermore, we find no support across multiple lines of evidence for inversions, which have long been assumed to halt recombination between the sex chromosomes. Conclusions: Our data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion and may result instead from the accumulation of transposable elements. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation and regulation of sex differentiation.

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

“…purpurea (Almeida et al 2020;Zhou et al 2020). No such gene is present in the Z-linked region of S. viminalis, consistent with the finding in the Populus species that the duplication is carried only in the Y-and not the X-linked region.…”

“…tremula (Müller et al 2020;Xue et al 2020). In two species of the Salix Chamaetia-Vetrix clade (S. purpurea and S. viminalis), a similar gene has been detected in the W-linked region of chromosome 15, and a partial and non-functional copy was found in the Z-linked region of the S. purpurea chromosome 15 (Almeida et al 2020;Yang et al 2020;Zhou et al 2020).…”

“…Although Salix is the largest genus in the family Salicaceae sensu lato, with ~450 species (reviewed in He et al 2020), fewer Salix than Populus genomes have been assembled, and assemblies include only the cushion shrub S. brachista and the shrub willows S. purpurea, S. suchowensis, and S. viminalis (Chen et al 2019;Almeida et al 2020;Wei et al 2020;Zhou et al 2020). Shrub stature is a derived character, and the tree habit is ancestral , and is usual in poplars.…”

Fine mapping of the sex locus in Salix triandra confirms a consistent sex determination mechanism in genus Salix

“…The chromosome number of willows and poplars is the same, and they do not exhibit a morphologically differentiated sex chromosome 9,10 . The Salicaceae family, whose young sex chromosomes have evolved from different autosomes, provides a valuable comparative system for studying sex differentiation in plants 11 . Multiple studies have reported that chromosome XIX is the incipient sex chromosome in poplars 12 , and both XX/ XY 13,14 and ZW/ZZ 12,15 sex determination systems have been observed in different poplar species.…”

“…Further study showed that the SDR in S. viminalis is of limited size (~804 kb) and exhibits a higher SNP density in females 25 . Pseudogenization and the accumulation of repetitive elements in the SDR suggest that the fundamental process of sex chromosome formation occurred very swiftly after recombination ceased 11 . In a recent study, the SDR of S. purpurea was found to contain large palindromic repeats, and the SpRR9 gene was considered a putative candidate for controlling sex determination through the modulation of the cytokinin signaling pathway 26 .…”