GIGANTEA functions as a co-repressor of cold stress response with a histone-modifying complex

Abstract

The circadian clock in plants is crucial for regulating stress responses, including cold tolerance. Cold stress induces the expression of C-REPEAT BINDING FACTOR (CBF) transcription factors, which activate COLD-REGULATED (COR) genes to mitigate cold-induced damage. Previously, we identified that HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE15 (HOS15)-HISTONE DEACETYLASE 2C (HD2C) complex regulates cold tolerance by modulating histone deacetylation on the COR genes. Our research reports that the circadian oscillator GIGANTEA (GI) regulates the association of histone deacetylase complex on the COR promoter, controlling cold tolerance. We show that GI functions downstream of HOS15, as the hos15-2 gi-2 double mutant exhibits freezing tolerance and expression of the COR gene like gi-2. Consistent with the HOS15, GI doesn't affect CBF transcription, suggesting that GI involved cold stress responses through HOS15-mediated COR gene regulation. Moreover, GI reduces histone acetylation and CBF binding at the COR15A promoter under cold stress, repressing COR15A gene expression. We further demonstrate that GI forms a co-repressor with HOS15 and HD2C, inhibiting CBF binding and preventing COR gene activation under normal conditions. These findings provide insights into molecular mechanisms by which GI, HOS15, and HD2C coordinate cold stress responses, offering potential strategies for enhancing plant cold tolerance through chromatin-mediated regulation.