CK2 kinase–PRC2 signalling regulates genome-wide H3K27 trimethylation and transduces prolonged cold exposure into epigenetic cold memory in plants

Abstract

Polycomb protein-mediated transcriptional repression plays a crucial role in the regulation of responses to environmental stimuli in multicellular eukaryotes, but the underlying signalling events remain elusive. During Arabidopsis vernalization, prolonged cold exposure results in the formation of a Polycomb-repressed domain at the potent floral repressor FLC to confer its stable silencing upon temperature rise or epigenetic ‘memory of prolonged cold’, enabling the plants to bloom in spring. Here we report that the evolutionarily conserved casein kinase CK2 phosphorylates and thus stabilizes histone 3 lysine-27 (H3K27) methyltransferases (PRC2 subunits) to promote H3K27 trimethylation throughout the Arabidopsis genome. We found that prolonged cold induces progressive CK2 accumulation, leading to a gradual accumulation of cellular PRC2. We further show that the cold-CK2–PRC2 signalling promotes increasing PRC2 enrichment on FLC chromatin during prolonged cold exposure as well as post-cold PRC2 spreading across FLC to establish a Polycomb-repressed domain for FLC repression in warmth. Thus, this signalling cascade transduces prolonged cold exposure, but not cold spells, into epigenetic memory of prolonged cold in warmth during vernalization. CK2 phosphorylation motifs are widely present in H3K27 methyltransferases from plants and animals. Our study reveals a new layer of control of PRC2 activity in multicellular organisms.