Epigenetically regulated transcriptional repressor, BASIC PENTACYSTEINE1 (BPC1) acts together with polycomb...

Camalexin is a phytoalexin produced by plants of the Brassicaceae family, including the model species Arabidopsis thaliana, and its biosynthesis is tightly regulated to balance growth and defense. Here, we identify BASIC PENTACYSTEINE 1 (BPC1) as a key negative regulator of camalexin biosynthesis. Transcriptome analyses of bpc1-1 and bpc1-1;bpc2-1 mutants revealed both distinct and overlapping functions of BPC1 and BPC2, with BPC1-specific differentially expressed genes being highly enriched for camalexin biosynthetic processes. Consistently, multiple camalexin pathway genes were upregulated in bpc1-1, leading to increased camalexin accumulation. Analysis of publicly available ChIP-seq data together with mutant expression profiles showed that several BPC1-regulated camalexin biosynthetic genes are enriched for the repressive histone mark, H3K27me3 and are de-repressed in Polycomb Repressive Complex 2 (PRC2) mutants, indicating PRC2-dependent transcriptional silencing. ChIP-qPCR analyses further demonstrated that BPC1 directly binds GA-rich cis-elements in camalexin pathway genes, including CYP71A12 and CYP71B15. Furthermore, epigenome profiling showed that the BPC1 locus itself is embedded within an active chromatin environment enriched in H3K4me2/3, H3K36me3, and histone acetylation. Loss-of-function mutants of histone H3 methyltransferases like ATX1, ATX2, ATXR7, and EFS exhibited reduced BPC1 expression, whereas a knock-out mutant of a histone H3 acetyltransferase gene, HDA9, hda9-1 displayed elevated H3ac levels and increased BPC1 transcript abundance, indicating that BPC1 transcription is epigenetically modulated by both histone methylation and acetylation dynamics. Together, our findings establish BPC1 as an epigenetically regulated transcriptional repressor that partners with PRC2 to suppress camalexin biosynthesis, revealing a previously unrecognized regulatory module controlling the basal suppression of specialized defensive metabolism in Arabidopsis.