Remarkable Divergence of the Sex-Linked Region between Two Wild Spinach Progenitors, Spinacia turkestanica and Spinacia tetrandra

Abstract

The sex-linked region (SLR) plays an important role in determining the sex of a plant. The SLR of the Y chromosome, composed of a 14.1-Mb inversion and a 10-Mb Y-duplication region (YDR), was deciphered in Spinacia oleracea previously. However, our understanding of the SLR in its wild relatives, S. turkestanica and S. tetrandra, remains limited. In this study, we used 63 resequencing data from the three Spinacia species to infer the evolution of the SLR among the Spinacia species. In the SLR, all the cultivated spinach and S. turkestanica accessions were clustered into two distinct categories with both sexes, while the S. tetrandra accessions of both sexes were grouped. This suggests that S. oleracea shared a similar SLR with S. turkestanica, but not with S. tetrandra, which was further confirmed based on the population structure and principal component analysis. Furthermore, we identified 3910 fully sex-linked SNPs in S. oleracea and 92.82% of them were available in S. turkestanica, while none of the SNPs were adopted in S. tetrandra. Genome coverage in males and females supported the hypothesis that the YDR increasingly expanded during its evolution. Otherwise, we identified 13 sex-linked transposable element insertion polymorphisms within the inversion in both S. oleracea and S. turkestanica, demonstrating that the transposable element insertions might have occurred before the recombination suppression event of the inversion. The SLR was conserved compared with the pseudoautosomal region given that the genetic hitchhiking process occurred in the SLR during its evolution. Our findings will significantly advance our understanding of the characteristics and evolution of the SLR in Spinacia species.

A rapid method for assembly of single chromosome and identification of sex determination region based on single‐chromosome sequencing

“…S. oleracea L. subsp. turkestanica also shared a similar sex‐linked region (SLR) with S. oleracea (She et al ., 2022). These may be because S. oleracea L. subsp.…”

“…However, the sex chromosome pairs in the part of S. tetrandra accessions are heteromorphic. In 2022, She et al . reported that S. oleracea shared a similar sex‐linked region with S. oleracea L. subsp.…”

Two wildSpinaciaspecies,S. turkestanicaandS. tetrandra, genomes reveal a sex chromosome turnover in the genus

“…S. turkestanica is the closest wild relative of S. oleracea , and these species share a similar SLR on chromosome 4 (She et al, 2022b). We used synteny analysis to describe the S. turkestanica SLR in detail.…”

“…We found orthologs of 35 S. oleracea YDR genes in the S. tetrandra assembly, but they are scattered across the genome (Supplementary Table 4), consistent with the previous conclusion that most S. oleracea YDR genes were recently translocated into the region (She et al, 2023). We previously described complete male-specificity of the YY_141140.1 gene (coding sequence length: 414 bp) within the YDRs of both S. oleracea and S. turkestanica (She et al, 2022b). A phylogenetic tree of YY_141140.1 and its orthologs shows that the relationships of the four outgroup species do not correspond with the species tree (Fig.…”

Gap‐free X and Y chromosome assemblies of Salix arbutifolia reveal an evolutionary change from male to female heterogamety in willows, without a change in the position of the sex‐determining locus

“…The single gene systems that have recently been discovered (Akagi et al, 2014;Muller et al, 2020), including new ones generated by sex chromosome turnovers (Vicoso, 2019), will not be selected for changed recombination (reviewed in Charlesworth & Harkess, 2024). Moreover, Y-and X-linked regions can also arise if sex-determining mutations arise within a recombinationally inactive region (Charlesworth, 2019) and examples of sex-linked regions (SLRs), within pericentromeric regions are now known in several plants (Zhou et al, 2018;Rifkin et al, 2021;She et al, 2023;Yue et al, 2023).…”