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 known to be tightly regulated, but the underlying molecular mechanisms remain unclear. Here, we report that a regulatory module composed of the DNA-binding protein VAL1 (VIVIPAROUS1/ABI3-LIKE 1) and an SIN3 (SWI-INDEPENDENT 3)-like histone deacetylase complex, dynamically regulates anthocyanin biosynthesis in Arabidopsis. 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, resulting in its potent transcriptional repression to inhibit anthocyanin biosynthesis. In response to JA rise, JAZs are degraded, and both VAL1 and SNL-HDA19c are released from PAP1 chromatin, leading to an immediate increase in histone acetylation to promote transcriptional activation of PAP1 and anthocyanin production. These findings elucidate a regulatory module (VAL1-JAZ-SNL-HDA19c) for the inhibition of anthocyanin biosynthesis under normal growth condition and further reveal how the stress hormone JA rapidly induces anthocyanin production, enabling that plants adapt to their growth conditions.