Chromosome-scale assemblies of the male and female Populus euphratica genomes reveal the molecular basis of sex determination and sexual dimorphism

Abstract

Reference-quality genomes of both sexes are essential for studying sex determination and sex-chromosome evolution, as their gene contents and expression profiles differ. Here, we present independent chromosome-level genome assemblies for the female (XX) and male (XY) genomes of desert poplar (Populus euphratica), resolving a 22.7-Mb X and 24.8-Mb Y chromosome. We also identified a relatively complete 761-kb sex-linked region (SLR) in the peritelomeric region on chromosome 14 (Y). Within the SLR, recombination around the partial repeats for the feminizing factor ARR17 (ARABIDOPSIS RESPONSE REGULATOR 17) was potentially suppressed by flanking palindromic arms and the dense accumulation of retrotransposons. The inverted small segments S1 and S2 of ARR17 exhibited relaxed selective pressure and triggered sex determination by generating 24-nt small interfering RNAs that induce male-specific hyper-methylation at the promoter of the autosomal targeted ARR17. We also detected two male-specific fusion genes encoding proteins with NB-ARC domains at the breakpoint region of an inversion in the SLR that may be responsible for the observed sexual dimorphism in immune responses. Our results show that the SLR appears to follow proposed evolutionary dynamics for sex chromosomes and advance our understanding of sex determination and the evolution of sex chromosomes in Populus.

Gap-free X and Y chromosomes ofSalix arbutifoliareveal an evolutionary change from male to female heterogamety in willows, without a change in the sex-determining region

“…The Salicaceae are therefore an interesting family, as turnovers have occurred, creating young sex-determining regions. Strata may have formed in the SLR of Populus euphratica , and an inversion detected in the assembly could have been involved, as the estimated mean divergence for genes within the inversion was 4%, versus only 0.018 for the rest of the SLR (Zhang et al, 2022b); however definitive evidence has not yet been published. In Salix viminalis , two evolutionary strata were identified, but the assemblies were low-quality, especially in the sex-linked region; moreover, the authors concluded that recombination may not be completely suppressed (Almeida et al, 2020).…”

Male-Specific Sequence in Populus simonii Provides Insights into Gender Determination of Poplar

“…Identifying sex-determining regions and genes is key to understanding the formation and evolution of sex chromosomes. However, sex-determining regions usually have a high repeat density, which means that the assembly process is difficult [36,37]. Previous genetic mapping studies have mapped the sex-determining region of poplar to the proximal telomeric end or centromere region of chromosome 19 [24,35].…”

The chromosome-scale genome and population genomics reveal the adaptative evolution of Populus pruinosa to desertification environment

“…The neutral mutation rate of 2.5 × 10 −9 mutations per bp per year was used [ 61 ]. The nonsynonymous (Ka) and synonymous (Ks) substitution rates of homologous gene pairs between P. pruinosa and P. euphratica [ 86 ] were calculated by PAML v4.9 [ 87 ]. GO enrichment of genes were performed using the R package clusterProfiler [ 88 ].…”