Maternal transmission of the epigenetic 'memory of winter cold' in Arabidopsis

Some plants can 'remember' past environmental experience to become adapted to a given environment. For instance, after experiencing prolonged low-temperature exposure in winter (winter cold), vernalization-responsive plants remember past cold experience when temperature rises in spring, to acquire competence to flower at a later season favourable for seed production^1,2. In Arabidopsis thaliana, prolonged cold induces silencing of the potent floral repressor FLOWERING LOCUS C (FLC) by Polycomb group (PcG) chromatin modifiers. This Polycomb-repressed chromatin state is epigenetically maintained and thus 'memorized' in subsequent growth and development upon return to warmth^1,3. 'Memory of winter cold' has been viewed as being mitotically stable but meiotically unstable^3-5, and thus not to be transmitted intergenerationally. In general, whether and how chromatin-mediated environmental memories are transmitted across generations are unknown in plants. Here, we show that the cold-induced Polycomb-repressed chromatin state at FLC or memory of winter cold is maintained in the egg cell, that is meiotically stable in the process of female gamete formation, and provide evidence that this Polycomb-mediated memory is not maintained in the sperm cell. Moreover, we show that this cold memory is inherited maternally but not paternally to the zygote and early embryos. Our study demonstrates and further provides mechanistic insights into intergenerational transmission of chromatin state-mediated environmental memories in plants.