Genome sequence of the wild species, <i>Spinacia tetrandra</i>, including a phased sequence of the extensive sex‐linked region, revealing partial degeneration in evolutionary strata with unusual properties

Genetic degeneration is a striking feature of Y chromosomes, often involving losses of many genes carried on the X chromosome. However, the time course of gene losses remains unclear. Sex chromosomes of plants evolved more recently than animals' highly degenerated ones, making them ideal for studying degeneration timing. To investigate Spinacia sex chromosome evolution and the time course of degeneration, we compared genome sequences of cultivated Spinacia oleracea, with a small Y-linked region on Chr4, with its two wild relatives. In spinach and its closest relative Spinacia turkestanica, the Y duplication region (YDR) introduced a male-determining factor into Chr4's low-recombining pericentromeric region. In other words, a turnover event occurred in these species' recent common ancestor. The homologous Chr4 of the more distantly related S. tetrandra has a c. 133 Mb completely sex-linked and partially degenerated region, possibly reflecting the ancestral state. Sequence divergence analysis suggests that two 'evolutionary strata' evolved shortly before the two Spinacia lineages split. Consistent with the turnover hypothesis, the YDR of the other two Spinacia species is not within the S. tetrandra older stratum. We discuss the unexpected findings in S. tetrandra that genetic degeneration, genomic rearrangements, and repetitive sequence density are all greatest in the younger stratum.