Integrative omic and transgenic analyses reveal methyl jasmonate- and abscisic acid-responsive regulator CwbHLH2 that positively regulates terpenoid biosynthesis in Curcuma wenyujin

Abstract

Bioactive terpenoids from Curcuma wenyujin (CW), as specialized metabolites, have huge medicinal properties. Accumulating evidence suggested that Jasmonates (JAs) and abscisic acid (ABA) shake hands and coordinately control a wide range of plant growth and defense activities, including the production of specialized metabolites. However, knowledge of how JA and ABA signalings interact to regulate terpenoid biosynthesis (TBS) is limited. In this study, integrative transcriptome and metabolome analyses revealed that exogenous methyl jasmonate (MeJA) and ABA activate the biosynthesis of terpenoids by upregulating the expressions of genes related to the TBS pathway, JA and ABA responses. Most of the differentially changed terpenoids and transcripts were commonly induced by MeJA and ABA. Interactive networks of “gene-gene/metabolite” indicated that CwbHLH2, a MeJA and ABA dual-responsive regulator, is tightly related to terpenoid production. Furthermore, transgenic experiments revealed that overexpression and RNA interference of CwbHLH2 upregulated and downregulated the contents of representative terpenoids in the MeJA- and ABA-treated transgenic hairy roots, respectively, with 1.52–3.06-fold increases and 29.6–68.7% reduction. Importantly, the genetic transformation of CwbHLH2 enhanced the expressions of multiple TBS pathway genes and bidirectionally enlarged the JA and ABA signalings caused by MeJA or ABA, demonstrating that CwbHLH2 plays a critical interrelational role in integrating MeJA- and ABA-induced TBS regulation. Altogether, our results not only advance a new view of the crosstalk between JA and ABA in modulating TBS but also provide a powerful strategy for improving the yield of bioactive terpenoids in CW.