Non-canonical RNA-directed DNA methylation participates in maternal and environmental control of seed dormancy

Seed dormancy is an adaptive trait preventing premature germination out of season. In a previous report (Piskurewicz et al., 2016) we showed that dormancy levels are maternally inherited through the preferential maternal allele expression in the seed endosperm of ALLANTOINASE (ALN), a negative regulator of dormancy. Here we show that suppression of ALN paternal allele expression is imposed by non-canonical RNA-directed DNA methylation (RdDM) of the paternal ALN allele promoter. Dormancy levels are further enhanced by cold during seed development. We show that DNA methylation of the ALN promoter is stimulated by cold in a tissue-specific manner through non-canonical RdDM, involving RDR6 and AGO6. This leads to suppression of ALN expression and further promotion of seed dormancy. Our results suggest that tissue-specific and cold-induced RdDM is superimposed to parental allele imprints to deposit in the seed progeny a transient memory of environmental conditions experienced by the mother plant.