Antagonistic regulation of anthocyanin biosynthesis by HY5 and BPC1 in Arabidopsis thaliana

Anthocyanins are flavonoid pigments that contribute to plant stress tolerance and environmental acclimation, yet how transcriptional activation is balanced with chromatin-based repression to fine-tune anthocyanin biosynthesis remains poorly understood. Here, we identify BASIC PENTACYSTEINE 1 (BPC1) as a key epigenetic repressor of anthocyanin biosynthesis in Arabidopsis thaliana . Transcriptome profiling of the bpc1-1 mutant revealed strong upregulation of anthocyanin biosynthetic and regulatory genes, accompanied by increased anthocyanin accumulation. Analysis of a genome-wide H3K27me3 ChIP-seq dataset in Col-0 wild type showed that many anthocyanin pathway genes are substantially enriched for H3K27me3 and are directly regulated by the Polycomb Repressive Complex 2 (PRC2), including LHP1. BPC1 is required for proper H3K27me3 deposition, thereby maintaining transcriptional repression under non-inductive conditions. In contrast, BPC1 is dispensable for PRC1-mediated H2A mono-ubiquitination at these loci. We further demonstrate that the light-responsive transcription factor, ELONGATED HYPOCOTYL 5 (HY5) directly associates with multiple regulatory and biosynthetic genes in the anthocyanin pathway and promotes their expression primarily through coordination of histone acetylation, rather than by altering H3K27me3 levels. Loss of HY5 leads to reduced histone acetylation and attenuated anthocyanin accumulation without broadly affecting PRC2-mediated repression. Together, our findings support a model in which anthocyanin biosynthesis is governed by a constitutive antagonistic interplay between BPC1-mediated PRC2 repression and HY5-driven transcriptional activation under non-stressed conditions. This basal chromatin regulatory state likely serves as a molecular pre-set for rapid induction of the anthocyanin pathway in response to environmental stimuli such as UV-B radiation, providing new insight into the epigenetic coordination of secondary metabolism in plants.