A histone deacetylase complex regulates anthocyanin biosynthesis during normal plant growth and development and in response to jasmonate

Anthocyanins are plant pigments that play diverse roles in plant growth, adaptation, and stress tolerance. Anthocyanin biosynthesis is tightly regulated, but the underlying regulatory mechanisms remain unclear. Here, we identify a regulatory module composed of the DNA-binding protein VAL1 (VIVIPAROUS1/ABI3-LIKE 1) and a SIN3 (SWI-INDEPENDENT 3)-like histone deacetylase complex that dynamically regulates anthocyanin biosynthesis in Arabidopsis thaliana. Under normal growth conditions, VAL1 recruits the SNL (SIN3-Like)-HDA19 (HISTONE DEACETYLASE 19) complex (SNL-HDA19c) to the PRODUCTION OF ANTHOCYANIN PIGMENT 1 (PAP1) locus for histone deacetylation. Moreover, the negative regulators of jasmonic acid (JA) signaling, JASMONATE-ZIM DOMAIN (JAZ) proteins, interact with VAL1 and further stabilize the binding of VAL1 and SNL-HDA19c to PAP1 chromatin. These molecular interactions transcriptionally repress PAP1 and inhibit anthocyanin biosynthesis. Upon JA accumulation, JAZs are degraded, resulting in the release of both VAL1 and SNL-HDA19c from the PAP1 chromatin. This release leads to an immediate increase in histone acetylation, promoting transcriptional activation of PAP1 and anthocyanin production. These findings elucidate a regulatory module (VAL1-JAZ-SNL-HDA19c) that represses anthocyanin biosynthesis under normal growth conditions and further reveal how the stress hormone JA rapidly induces anthocyanin production, enabling plants to adapt to their growth conditions.