Random epigenetic inactivation of the X-chromosomal HaMSter gene causes sex ratio distortion in persimmon

Abstract

In contrast to the recent progress in the genome sequencing of plant sex chromosomes, the functional contribution of the genes in sex chromosomes remains little known1. They were classically thought to be related to sexual dimorphism, which is beneficial to male or female functions, including segregation ratios. Here we focused on the functional evolution of the sex ratio distortion-related locus Half Male Sterile/Inviable (HaMSter), which is located in the short sex-linked region in diploid persimmon (Diospyros lotus). The expression of HaMSter, encoding a plant1589-like undefined protein, is necessary for production of viable seeds. Notably, only X-allelic HaMSter is substantially expressed and half of the maternal X alleles of HaMSter is randomly inactivated, which results in sex ratio distortion in seeds. Genome-wide DNA methylome analyses revealed endosperm-specific DNA hypermethylation, especially in the X-linked region. The maintenance/release of this hypermethylation is linked to inactivation/activation of HaMSter expression, respectively, which determines the sex ratio distortion pattern. The sex ratio is often not even in plants, and its molecular mechanisms have been little known. The study found that an X chromosome-encoded gene, named HaMSter in persimmon, influences sex ratio distortion via seed viability through a regulatory mechanism involving random DNA methylation.