The female (XX) and male (YY) genomes provide insights into the sex determination mechanism in spinach

Abstract

Sexual reproduction is the primary means of reproduction for the vast majority of macroscopic organisms, including almost all animals and plants. Sex chromosomes are predicted to play a central role in sexual dimorphism. Sex determination in spinach is controlled by a pair of sex chromosomes. However, the mechanisms of sex determination in spinach remain poorly understand. Here, we assembled the genomes of both a female (XX) and a male (YY) individual of spinach, and the genome sizes were 978 Mb with 28,320 predicted genes and 926 Mb with 26,537 predicted genes, respectively. Based on reported sex-linked markers, chromosomes 4 of the female and male genome were defined as the X and Y chromosomes, and a 10 Mb male-specific region of the Y chromosome (MSY) from approximately 95– 105 Mb, was identified that contains abundant transposable elements (92.32%). Importantly, a large-scale inversion of about 13 Mb in length was detected on the X chromosome, corresponding to ~9 Mb and ~4 Mb on the Y chromosome, which were located on both sides of the MSY with two distinct evolutionary strata. Almost all sex-linked/Y-specific markers were enriched on the inversions/MSY, suggesting that the flanked inversions might result in recombination suppression between the X and Y chromosomes to maintain the MSY. Forty-nine genes within the MSY had functional homologs elsewhere in the autosomal region, suggesting movement of genes onto the MSY. The X and Y chromosomes of spinach provide a valuable resource for investigating spinach sex chromosomes evolution from wild to cultivated spinach and also provide a broader understanding of the sex determination model in the Amaranthaceae family.

The Diversity of Plant Sex Chromosomes Highlighted through Advances in Genome Sequencing

“…All three species of Spinacia (Amaranthaceae) are dioecious, and though S. oleracea and S. tetrandra diverged ~5.7 MYA, analyses of sex-linked homologs suggest suppressed recombination occurred after their divergence [ 167 ]. Recent analyses in S. oleracea have found the SDR to be between 10–19 Mb, with a 10 Mb MSY that has 210 genes [ 109 , 168 ]. These genes have been captured into the region of suppressed recombination through chromosomal inversions, making two strata of divergence between the X and the Y [ 109 ].…”

“…Recent analyses in S. oleracea have found the SDR to be between 10–19 Mb, with a 10 Mb MSY that has 210 genes [ 109 , 168 ]. These genes have been captured into the region of suppressed recombination through chromosomal inversions, making two strata of divergence between the X and the Y [ 109 ]. The 12 MSY genes with putative floral functions [ 109 ] and additional transcriptomic analyses of female and male flowers [ 169 ] have narrowed in potential sex-determining genes, though none so far are clear candidates.…”

“…Multiple recombination-suppression events thus show a stepwise pattern of Ks along the SDR, with lower Ks for more-recent captures and higher Ks for older-captured genes. Indeed, evidence of evolutionary strata has been found in several plant species [ 69 , 87 , 109 ], suggesting plants may experience similar selective pressures that drive gene gain as animals [ 203 ]. The structural changes that cause suppressed recombination have classically been shown to be chromosomal inversions and several recent papers have found evidence in plants to also support this [ 109 , 204 ].…”

“…Indeed, evidence of evolutionary strata has been found in several plant species [ 69 , 87 , 109 ], suggesting plants may experience similar selective pressures that drive gene gain as animals [ 203 ]. The structural changes that cause suppressed recombination have classically been shown to be chromosomal inversions and several recent papers have found evidence in plants to also support this [ 109 , 204 ]. Some other striking convergent patterns, like palindromes, have been found in animal and plant sex chromosomes [ 94 , 147 ].…”

The diversity of plant sex chromosomes highlighted through advances in genome sequencing

“…Spinach: All three species of Spinacia (Amaranthaceae) are dioecious, and though S. oleracea and S. tetrandra diverged ~5.7 MYA, analyses of sex-linked homologs suggest suppressed recombination occurred after their divergence [127]. Recent analyses in S. oleracea have found the SDR to be between 10-19 Mb, with a 10 Mb MSY that has 210 genes [128,129]. These genes have been captured into the region of suppressed recombination through chromosomal inversions, making two strata of divergence between the X and the Y [129].…”