The Polycomb-group chromatin modifiers play important roles to repress or switch off gene expression in plants and animals. How the active chromatin state is switched to a Polycomb-repressed state is unclear. In Arabidopsis , prolonged cold induces the switching of the highly active chromatin state at the potent floral repressor FLC to a Polycomb-repressed state, which is epigenetically maintained when temperature rises to confer "cold memory," enabling plants to flower in spring. We report that the cis -acting cold memory element (CME) region at FLC bears bivalent marks of active histone H3K4me3 and repressive H3K27me3 that are read and interpreted by an assembly of bivalent chromatin readers to drive cold-induced switching of the FLC chromatin state. In response to cold, the 47-bp CME and its associated bivalent chromatin feature drive the switching of active chromatin state at a recombinant gene to a Polycomb-repressed domain, conferring cold memory. We reveal a paradigm for environment-induced chromatin-state switching at bivalent loci in plants. [Display omitted] • Cold memory element (CME) at FLC is associated with bivalent histone marks • Dual histone readers (EBS and SHL) form dimers to read H3K4me3 and H3K27me3 • DNA-binding protein VAL1 recognizes CME and interacts with EBS and SHL • CME-VAL1-EBS/SHL-PRC2 drives long cold-induced chromatin state switching Gao et al. report that a 47-bp DNA element together with its associated bivalent chromatin feature at the floral repressor FLC drives the switching of an active chromatin state to Polycomb-repressed domain in response to prolonged cold exposure, which is stably maintained during post-cold growth and development to confer "memory of prolonged cold" in Arabidopsis. [ABSTRACT FROM AUTHOR]