Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies.