BAHD acyltransferase induced by histone deacetylase inhibitor catalyzes 3‐O‐hydroxycinnamoylquinic acid formation in bamboo cells

SUMMARY Suspension‐cultured cells of a bamboo species (Bambusa multiplex; Bm) produce 3‐O‐feruloylquinic acid (3‐FQA) and 3‐O‐p‐coumaroylquinic acid (3‐pCQA) by treatment with the histone deacetylase inhibitor suberoyl bis‐hydroxamic acid (SBHA). Acyltransferases catalyzing the formation of 5‐O‐hydroxycinnamoylquinic acid esters by transesterification from hydroxycinnamoyl‐CoAs to the C‐5 hydroxy group of quinic acid (hydroxycinnamoyl‐CoA:quinate hydroxycinnamoyltransferase, HQT) have been identified in the biosynthesis of chlorogenic acids and monolignols; however, an HQT that catalyzes the acylation of the C‐3 hydroxy group of quinic acid has not been identified previously. In the present study, we purified a native HQT from SBHA‐treated Bm cells. The purified enzyme preferentially accepted feruloyl‐/p‐coumaroyl‐CoAs as acyl‐donors and quinic acid as the acyl‐acceptor, and the enzyme specifically formed 3‐FQA and 3‐pCQA but not 5‐O‐hydroxycinnamoylquinic acid esters or esters with shikimic acid. A cDNA (BmHQT1) encoding this HQT was isolated. Although BmHQT1 is a phylogenetically unique member of the BAHD acyltransferase superfamily that does not cluster with other HQTs, functional characterization of the recombinant enzyme verified that BmHQT1 catalyzes the regiospecific formation of 3‐O‐hydroxycinnamoylquinic acid esters. Transcript levels of BmHQT1 markedly increased in Bm cells cultured in the presence of SBHA. Moreover, elevated acetylation levels of histone H3 were observed in the coding region of BmHQT1 in the presence of SBHA, indicating that the induced accumulation of 3‐FQA/3‐pCQA by SBHA is caused by transcriptional activation of BmHQT1 by the action of SBHA as a histone deacetylase inhibitor. The results demonstrate the utility of HDAC inhibitors for discovery of cryptic secondary metabolites and unknown biosynthetic enzymes. Significance Statement Identification of a BAHD acyltransferase catalyzing the formation of 3‐O‐hydroxycinnamoylquinic acid esters significantly contributes to understanding the entire biosynthetic pathway of chlorogenic acids and the functional diversity of BAHD acyltransferases because only BAHD acyltransferases catalyzing the formation of 5‐O‐hydroxycinnamoylquinic acid esters have been identified previously. The present study shows the utility of the treatment of plant cells with histone deacetylase inhibitors for the discovery of cryptic secondary metabolites and hitherto unknown secondary metabolite biosynthetic en