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

Global warming increasingly threatens agricultural productivity, necessitating the development of new crop varieties that combine high yield potential with climate resilience. Optimizing plant architecture, particularly by reducing leaf angle (LA), enables dense planting and enhances light capture, yet the mechanisms that coordinate architectural improvement with heat tolerance remain largely unknown. Here, we identify the microRNA ZmMIR319A as a key regulator of both LA and thermotolerance in maize. ZmMIR319A increases LA by post-transcriptionally repressing the Teosinte branched1/Cycloidea/PCF (TCP) transcription factors ZmTCP5 and ZmTCP44, thereby relieving their suppression of the auxin transporter genes ZmPIN1 and ZmPIN8 and stimulating parenchyma cell proliferation in the ligular region. Under heat stress, rapid downregulation of ZmMIR319A leads to the accumulation of ZmTCP5 and ZmTCP44 proteins, which repress 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 maize ZmMIR319A-ZmTCP5/44 module bifurcates into two regulatory pathways that coordinately govern LA through auxin transport and thermotolerance through heat shock protein signaling. Notably, ZmMIR319A-knockout mutants exhibit 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 simultaneously controls plant architecture and stress adaptation, thereby providing a dual-target strategy for the molecular breeding of maize varieties with ideal plant architecture and climate resilience.