SWI3b restricts AGO5 expression to promote the initiation of megagametogenesis in Arabidopsis

Female germline development is fundamental to plant reproduction. During megasporogenesis, a somatic ovule cell differentiates into a megaspore mother cell (MMC) and undergoes meiosis to produce a single haploid megaspore while three spores degenerate. The surviving functional megaspore undergoes three rounds of mitosis during the process of megagametogenesis to produce the seven-celled female gametophyte or embryo sac. The mechanism by which the functional megaspore initiates gametogenesis remained unclear. Here, we show that the chromatin remodelling protein SWI3b is required for the initiation of megagametogenesis, but not for megasporogenesis. SWI3b activity either in the MMC or somatic ovule primordium cells alone is not sufficient for the initiation of megagametogenesis. We identified AGO5 as a direct target of SWI3b, which restricts AGO5 expression to the nucellus. We further show that SWI3b is required for maintaining low histone H3 lysine 9 acetylation level at the AGO5 locus, while elevated AGO5 abundance in the nucellus disrupts the initiation of megagametogenesis. In summary, our study reveals that SWI3b promotes the initiation of megagametogenesis through chromatin-mediated repression of AGO5 , leading to its exclusion from the MMC and thereby linking histone acetylation and epigenetic mechanisms to the development of the female germ cells.