The ZmMIR319A-ZmTCP5/44 module bifurcates into two pathways to coordinately regulate leaf angle and thermotolerance...

Global warming increasingly threatens crop productivity, necessitating new varieties that combine high yield potential with climate resilience. Optimizing plant architecture, particularly by reducing leaf angle (LA), enables dense planting and enhanced light capture, yet the mechanisms coordinating architecture improvement with heat tolerance remain largely unknown. Here, we identify the microRNA ZmMIR319A as a key regulator that simultaneously regulates LA and thermotolerance in maize. ZmMIR319A promotes LA by post-transcriptionally repressing Teosinte branched1/Cycloidea/PCF (TCP) transcription factors ZmTCP5 and ZmTCP44, thereby relieving their suppression of auxin transporter genes ZmPIN1 and ZmPIN8 to stimulate parenchyma cell proliferation in the ligular region. Under heat stress, rapid downregulation of ZmMIR319A leads to accumulation of ZmTCP5/44 proteins, which suppress the heat shock chaperone genes ZmHSP70-4 and ZmHSP90-5 in leaves to modulate thermotolerance, while continuing to restrain ZmPIN1/8-mediated growth. Thus, the ZmMIR319A-ZmTCP5/44 module bifurcates into two pathways in maize that coordinately govern LA via auxin transport and thermotolerance via heat shock protein signaling. Notably, ZmMIR319A knockout mutants achieve increased grain yield under high-density planting conditions despite reduced thermotolerance, highlighting a trade-off between architectural optimization and stress adaptation. Collectively, our findings reveal that a single regulatory module can simultaneously optimize plant architecture and stress adaptation, providing a dual-target strategy for molecular breeding of maize varieties with ideal plant architecture and climate resilience.