Mayang Liu, Yingda Huang, Zheng Li, Xuanlong Lv, Mingqi Gu, Shuhua Liao, Xin Dong, Yingbo Gao, Zhen Gao, Pu Wang, Shoubing Huang
High temperature (HT, ≥ 38°C) impairs maize (Zea mays L.) yield by disrupting pollination, yet mechanisms in female reproductive organs remain elusive. Maize silks, the essential tissues for pollen capture and pollen tube growth, are particularly sensitive to HT, are highly vulnerable to HT. Here, we combined phenotypic, physiological, metabolic and transcriptomic analyses under controlled HT (40/30°C) and control (32/22°C) conditions to dissect mechanisms underlying HT-induced silk growth inhibition (SGI) and silk pollination dysfunction (SPD). HT reduced silk emergence by ~20% but decreased seed set by ~50%, indicating SPD dominated kernel loss over SGI. HT significantly downregulated key genes of the silks that encode sucrose transporters, sugars will eventually be exported through transporters and glycolytic enzymes (hexokinase; 6-phosphofructokinase; pyruvate kinase), restricting energy metabolism required for silk elongation and pollen tube growth. Concurrently, HT elevated abscisic acid and indole-3-acetic acid while suppressing zeatin riboside, brassinolide and jasmonic acid levels, collectively driving SGI. SPD was primarily linked to oxidative damage via suppressed flavonoid biosynthesis (chalcone synthase, flavonol synthase and peroxidase) and impaired reactive oxygen species (ROS) scavenging. Specifically, HT induced a negative correlation between ZmARF1 and ZmSOD3 expression, suggesting compromised ROS clearance that exacerbated silk structural damage. These findings provide new insights into the metabolic, hormonal and transcriptional regulatory networks that govern silk thermotolerance, providing potential molecular targets for breeding heat-resilient maize varieties.