bHLH19 and bHLH20 repress jasmonate-mediated plant defense against insect herbivores in Arabidopsis

Plants are attacked by various insect herbivores. Upon attack-triggered biosynthesis of the phytohormone jasmonates (JAs), the JA receptor CORONATINE INSENSITIVE 1 recruits the JA-ZIM domain (JAZ) repressors for ubiquitination, releases the MYC-MYB transcription factor (TF) complexes, and enhances glucosinolates (GSs) biosynthesis to promote defense against insects in Arabidopsis. However, the negative regulation of JA-regulated defense remains largely unclear. Here, we found that Arabidopsis IVa bHLH TFs bHLH19 and bHLH20 interacted with JAZs. The bhlh19/20 mutations enhanced defense against the insects Spodoptera frugiperda and S. exigua, while their overexpression inhibited defense. bHLH19/20 repressed defense via at least two layers of regulation: first, bHLH19/20 interacted with the members MYC2/3/4/5 and MYB34/51/122 of MYC-MYB complexes, and inhibited the interaction/transcription activity of MYC2-MYB34; second, bHLH19/20 activated the RNA level of nitrile-specifier protein 1, which converts GSs into the less toxic nitriles. bhlh19/20 exhibited no penalty in JA-regulated growth inhibition. Collectively, our findings reveal the molecular mechanism for negatively regulating JA-mediated defense against insects in Arabidopsis without growth penalty by the pair of bHLH19/20 TFs.