Cold-induced H3K27me3 profiling reveals endospermic ARFs as regulators of seed dormancy, and of seed development and adaptation to cold

Abstract

Seed dormancy is an adaptive trait preventing germination out of season. Dormancy is implemented by the mature seed endosperm, which releases abscisic acid (ABA) upon imbibition. Dormancy levels are enhanced by cold temperatures, a major seasonal clue, during seed development. We found that cold-induced enhancement of dormancy requires CLF, a component of the Polycomb Repressive Complex 2 (PRC2), which mediates H3K27me3 deposition. Cold-induced H3K27me3 profiling in the endosperm identified a family of highly homologous AUXIN RESPONSE FACTOR (ARF) genes clustered in the Arabidopsis genome and specifically expressed in the micropylar endosperm early during embryogenesis (referred as “EndoARFs”). EndoARFs are required to adjust seed dormancy levels in response to cold. They also redundantly promote embryo development beyond the globular stage, and their loss of function partially suppresses PRC2 mutant phenotypes, revealing a regulatory interplay between EndoARFs and PRC2. Cold-induced H3K27me3 deposition at EndoARF loci supports proper seed development under low temperatures, suggesting a mechanism by which epigenetic regulation adjusts embryogenesis to environmental conditions. Our results further support that successful seed formation in Arabidopsis thaliana depends on coordinated embryo and endosperm development.