Inhibiting reactive oxygen species production mitigates endoplasmic reticulum damage in florets of developing maize ears under heat stress

Heat stress is increasingly becoming a major constraint to agricultural production due to global warming and higher probability of extreme events. To mitigate the yield loss caused by heat stress, it is essential to understand the mechanisms underlying its effects on young ear development. In this study, we investigate the impact of heat stress on heat-sensitive and heat-tolerant maize varieties under field conditions. A combination of phenotypic, physiological, anatomical, and multi-omics techniques was used to assess the properties of young ears, from the phenotypic to molecular level, in response to heat stress during growth. The results show that heat stress primarily disrupts endoplasmic reticulum function in maize. Specifically, heat stress disrupts mitochondrial structure, and abnormalities in the electron transport chain lead to an increase in reactive oxygen species (ROS) levels, resulting in oxidative stress, protein unfolding, and cellular structure disruption. Consequently, the fertilization rate of florets and the number of grains per ear decrease by 16%-42% and 33%-54%, respectively, resulting in a 29%-60% overall yield loss. ZD-tol (heat-tolerant variety) demonstrated thermotolerance by more rapidly activating various pathways, such as protein catabolism, energy metabolism, carbohydrate metabolism, amino acid metabolism, and lipid metabolism, raising the threshold for stimuli detection and accelerating cellular ROS detoxification. Compared to ZD-tol, XY-sens (heat-sensitive variety) exhibits weaker cellular detoxification ability, thereby demonstrating heightened sensitivity to heat stress. However, the application of ROS inhibitors significantly reduces ROS levels in florets, alleviate endoplasmic reticulum stress, and decreased yield loss by 17%-31%, with XY-sens showing better mitigation effects compared to ZD-tol.