The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development

Abstract
Plants have evolved sophisticated systems for adaptation to their natural habitat. In response to developmental and environmental cues, plants produce and perceive jasmonate (JA) signals, which induce degradation of JASMONATE-ZIM-Domain (JAZ) proteins and derepress the JAZ-repressed transcription factors to regulate diverse aspects of defense responses and developmental processes. Here, we identified the bHLH subgroup IIId transcription factors (bHLH3, bHLH13, bHLH14 and bHLH17) as novel targets of JAZs. These bHLH subgroup IIId transcription factors act as transcription repressors and function redundantly to negatively regulate JA responses. The quadruple mutant bhlh3 bhlh13 bhlh14 bhlh17 showed severe sensitivity to JA-inhibited root growth and JA-induced anthocyanin accumulation, and exhibited obvious increase in JA-regulated plant defense against pathogen infection and insect attack. Transgenic plants overexpressing bHLH13 or bHLH17 displayed reduced JA responses. Furthermore, these bHLH factors functioned as transcription repressors to antagonize the transcription activators, such as MYC2 and the WD-repeat/bHLH/MYB complex, through binding to their target sequences. Coordinated regulation of JA responses by transcription activators and repressors would benefit plants by allowing fine regulation of defense and development, and survival in their frequently changing environment. Plants live in fixed places and have to evolve sophisticated systems for adaptation to their frequently changing environment. Plant hormones are essential for the regulation of these sophisticated systems which coordinately control plant growth, development, reproduction and defense. Jasmonates (JAs), a new class of cyclic fatty acid-derived plant hormone, regulate diverse aspects of plant defense and developmental processes. In response to external environmental signals and internal developmental cues, plants rapidly produce and efficiently perceive JA signals, which regulate a dynamic regulatory network to activate various downstream transcription factors essential for appropriate plant defense and development. Here, we identified the bHLH3, bHLH13, bHLH14 and bHLH17 transcription factors as novel transcription repressors of JA signaling. The coordinated regulation of JA-mediated plant defense and development by transcription activators and repressors would improve the survival of plants in their natural habitat and adaptation to the frequently fluctuating environment.