Jasmonic acid-mediated stress responses share the molecular mechanism underlying male sterility induced by deficiency of ZmMs33 in maize

Plant male reproduction is a fine-tuned developmental process that is susceptible to stressful environments and influences crop grain yields. Phytohormone signaling functions in control of plant normal growth and development as well as in response to external stresses, but the interaction or crosstalk among phytohormone signaling, stress response, and male reproduction in plants remains poorly understood. Cross-species comparison among 514 stress-response transcriptomic libraries revealed that ms33-6038, a genic male sterile mutant deficient in the ZmMs33/ZmGPAT6 gene, displayed an excessive drought stress-like transcriptional reprogramming in anthers triggered mainly by disturbed jasmonic acid (JA) homeostasis. An increased level of JA appeared in ZmMs33-deficient anthers at both meiotic and post-meiotic stages and activated genes involved in JA biosynthesis and signaling as well as genes functioning in JA-mediated drought response. Excessive accumulation of JA elevated expression level of a gene encoding a WRKY transcriptional factor that activated the ZmMs33 promoter. These findings reveal a feedback loop of ZmMs33-JA-WRKY-ZmMs33 in controlling male sterility and JA-mediated stress response in maize, shedding light on the crosstalk of stress response and male sterility mediated by phytohormone homeostasis and signaling.