Scientists at the Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences of the Chinese Academy of Sciences, discovered that a novel histone reader complex which can recognize H3K27me3 and repress transcription through dephosphorylation of Pol II. This study was published in Nature Communications.

H3K27me3 is an important histone post-translational modification (PTM) involving in the most biological processes. In traditional views, Polycomb Repressive Complex 2 (PRC2) was responsible for the deposition of H3K27me3 and PRC1 can bind H3K27me3, catalyzing H2Aub and further promoting chromatin condensation to block the accessibility of transcriptional complex. However, this model had been challenged by recent reports in which many new H3K27me3 reader components were found.

In this study, scientists identified a new protein complex containing BAH protein AIPP3, PHD protein AIPP2 or PAIPP2, and Pol II phosphatase CPL2 (BAH-PHD-CPL2 complex, BPC complex). The bpc mutants showed the photoperiod-independently early flowering time and developmental defect, indicating the indispensable role of BPC complex in plant development and flowering regulation. Genetic assays suggested that BPC regulates flowering through constitutively repression of FT expression.

Through structural and biochemical assays, they found that the AIPP3-BAH and the AIPP2/PAIPP2-PHD cooperate to read H3K27me3 and unmodified H3K4 histone marks, respectively, in Arabidopsis. ChIP-seq and mRNA-seq data showed that BPC complex directly binds and silences a substantial subset of H3K27me3-enriched loci, including a number of development and stress response-related genes. Interestingly, H3K27me3 deposition was not obviously changed between Col-0 and bpc mutants at selected target genes, indicating that BPC complex acts in downstream pathway of H3K27me3 deposition.

CPL2 has been reported as a plant-specific phosphatase to eliminate phosphorylation on the Ser5 (ser5P) of Pol II carboxyl terminal domain (CTD). Through a published NET-seq data of Pol II, scientists found that only a sharp peak of unphosphorylated Pol II signals was observed at the TSS region of the selected target genes but phosphorylated Pol II not, indicating BPC complex interrupts Pol II initiation rather than recruitment. They observed higher accumulations of phosphorylated Pol II in bpc mutants. More importantly, they found BAH-PHD module is indispensable for chromatin localization of CPL2.

This study first connected the recognition of H3K27me3 with Pol II dephosphorylation, suggesting a unique H3K27me3-mediated epigenetic silencing mechanism independent with canonical PRC2-PRC1-H2Aub pathway. Although CPL2 is a plant-specific phosphatase, the crosstalk between histone modification and Pol II CTD codes may exist widely in eukaryotic system.