Chromatin remodeling at the C-REPEAT BINDING FACTOR cluster controls growth retardation at low ambient temperature

Temperature impacts plant growth and development. However, the molecular mechanisms underlying growth retardation at low ambient temperature remain poorly understood. Here, we identify genetic and epigenetic determinants mediating growth retardation at low ambient temperature in Arabidopsis (Arabidopsis thaliana). Transcriptomic profiling showed that low ambient temperature (12 °C) upregulates regulatory genes associated with growth inhibition. We uncovered a regulatory network in which a Polycomb-Group (PcG) protein, VERNALIZATION INSENSITIVE 3-LIKE 1 (VIL1), and a transcription factor, C-REPEAT BINDING FACTOR 1 (CBF1), coordinate growth regulation under these conditions. The vil1 mutant displayed enhanced biomass, whereas cbf1 mutants showed the opposite phenotype at low ambient temperature. VIL1 establishes a repressive chromatin environment at the 3 tandemly clustered CBF locus, via H3K27me3 deposition and maintenance of noninductive chromatin structure. Upon low ambient temperature exposure, CBF chromatin transiently opens and forms loops to activate CBF genes. Increased VIL1 binding enhances H3K27me3 accumulation, fine-tuning CBF1 expression. Loss of VIL1 leads to reduced H3K27me3, increased chromatin accessibility, and persistent loop formation, resulting in elevated CBF1 expression. Our findings reveal that VIL1 modulates growth at low ambient temperature by regulating chromatin architecture and transcriptional activity, providing insights into how plants reprogram growth in response to low ambient temperature.