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

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.