MicroRNAs Regulate the Timing of Embryo Maturation in Arabidopsis

The seed is a key evolutionary adaptation of land plants that facilitates dispersal and allows for germination when the environmental conditions are adequate. Mature seeds are dormant and desiccated, with accumulated storage products that are to be used by the seedling after germination. These properties are imposed on the developing embryo by a maturation program, which operates during the later part of embryogenesis. A number of master regulators (the LEC genes) required for the induction of the maturation program have been described, but it is not known what prevents this program from being expressed during early embryogenesis. Here, we report that Arabidopsis (Arabidopsis thaliana) embryos mutant for strong alleles of DICER-LIKE1, the enzyme responsible for the biosynthesis of microRNAs (miRNAs), mature earlier than their wildtype counterparts. This heterochronic phenotype indicates that miRNAs are key regulators of the timing of the maturation program. We demonstrate that miRNAs operate in part by repressing the master regulators LEAFY COTYLEDON2 and FUSCA3 and identify the trihelix transcription factors ARABIDOPSIS 6B-INTERACTING PROTEIN1-LIKE1 (ASIL1) and ASIL2 and the histone deacetylase HDA6/SIL1 as components that act downstream of miRNAs to repress the maturation program early in embryogenesis. Both ASIL1 and HDA6/SIL1 are known to act to prevent the expression of embryonic maturation genes after germination, but to our knowledge, this is the first time they have been shown to have a role during embryogenesis. Our data point to a common negative regulatory module of maturation during early embryogenesis and seedling development.