Jasmonate mimic modulates cell elongation by regulating antagonistic bHLH transcription factors via brassinosteroid signaling

Lodging restricts growth, development, and yield formation in maize (Zea mays L.). Shorter internode length is beneficial for lodging tolerance. However, although brassinosteroids (BRs) and jasmonic acid (JA) are known to antagonistically regulate internode growth, the underlying molecular mechanism is still unclear. In this study, application of the JA mimic coronatine (COR) inhibited basal internode elongation at the jointing stage and repressed expression of the cell wall-related gene XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE 1 (ZmXTH1), whose overexpression in maize plants promoted internode elongation. We demonstrated that the basic helix-loop-helix (bHLH) transcription factor ZmbHLH154 directly binds to the ZmXTH1 promoter and induces its expression, whereas the bHLH transcription factor ILI1 BINDING BHLH 1 (ZmIBH1) inhibits this transcriptional activation by forming a heterodimer with ZmbHLH154. Overexpressing ZmbHLH154 led to longer internodes, whereas zmbhlh154 mutants had shorter internodes than the wild type. The core JA-dependent transcription factors ZmMYC2-4 and ZmMYC2-6 interacted with BRASSINAZOLE RESISTANT 1 (ZmBZR1), a key factor in BR signaling, and these interactions eliminated the inhibitory effect of ZmBZR1 on its downstream gene ZmIBH1. Collectively, these results reveal a signaling module in which JA regulates a bHLH network by attenuating BR signaling to inhibit ZmXTH1 expression, thereby regulating cell elongation in maize.