Epigenetic switch from repressive to permissive chromatin in response to cold stress

Significance

Phenotypic adaptations of plants in response to changes in climate are well known to be mediated by molecular mechanisms, including activation or suppression of transcription factors that control target gene expression. However, the chromatin changes that are essential for the binding of transcription factors are much less understood. Gene derepression at the chromatin level is considered to be the starting point for gene transcription. We report a mechanism of gene derepression through which HOS15 promotes the degradation of histone deacetylase HD2C in a cold-dependent manner that correlates with increased levels of acetylated histones on COR gene chromatin. Moreover, HOS15 directly promotes COR gene transcription by association of CBF transcription factors with the “open” state of the target COR chromatin.

Abstract

Switching from repressed to active status in chromatin regulation is part of the critical responses that plants deploy to survive in an ever-changing environment. We previously reported that HOS15, a WD40-repeat protein, is involved in histone deacetylation and cold tolerance in Arabidopsis. However, it remained unknown how HOS15 regulates cold responsive genes to affect cold tolerance. Here, we show that HOS15 interacts with histone deacetylase 2C (HD2C) and both proteins together associate with the promoters of cold-responsive COR genes, COR15A and COR47. Cold induced HD2C degradation is mediated by the CULLIN4 (CUL4)-based E3 ubiquitin ligase complex in which HOS15 acts as a substrate receptor. Interference with the association of HD2C and the COR gene promoters by HOS15 correlates with increased acetylation levels of histone H3. HOS15 also interacts with CBF transcription factors to modulate cold-induced binding to the COR gene promoters. Our results here demonstrate that cold induces HOS15-mediated chromatin modifications by degrading HD2C. This switches the chromatin structure status and facilitates recruitment of CBFs to the COR gene promoters. This is an apparent requirement to acquire cold tolerance.