Sporophyte-directed gametogenesis in Arabidopsis

Abstract

Plants alternate between diploid sporophyte and haploid gametophyte generations1. In mosses, which retain features of ancestral land plants, the gametophyte is dominant and has an independent existence. However, in flowering plants the gametophyte has undergone evolutionary reduction to just a few cells enclosed within the sporophyte. The gametophyte is thought to retain genetic control of its development even after reduction2. Here we show that male gametophyte development in Arabidopsis, long considered to be autonomous, is also under genetic control of the sporophyte via a repressive mechanism that includes large-scale regulation of protein turnover. We identify an Arabidopsis gene SHUKR as an inhibitor of male gametic gene expression. SHUKR is unrelated to proteins of known function and acts sporophytically in meiosis to control gametophyte development by negatively regulating expression of a large set of genes specific to postmeiotic gametogenesis. This control emerged late in evolution as SHUKR homologues are found only in eudicots. We show that SHUKR is rapidly evolving under positive selection, suggesting that variation in control of protein turnover during male gametogenesis has played an important role in evolution within eudicots. Ancestral land plants had a free-living gametophyte, but in flowering plants the gametophyte develops within the sporophyte. This study shows that male gametophyte development in Arabidopsis is directed by the sporophyte through repression of gametogenesis genes.