Crosstalk between physiological and genetic mechanisms during maintenance of acquired thermotolerance in tomato

Climate resilient crops are urgently needed to mitigate food insecurity arising from climate change and increased population. Enhancing plant stress memory is an efficient approach for improving crop resilience. We studied the underlying physiological and molecular mechanisms that accompany heat stress memory in tomato (Solanum lycopersicum L.). Compared to non-primed plants, heat primed plants exhibited improved morphological traits, leaf photosynthetic capacity, water utilization efficiency and water potential at 45 °C. Primed plants displayed a transient enhancement in reactive oxygen species (ROS) production together with higher antioxidant enzyme activity, leading to improved ROS homeostasis and reduced oxidative damage during prolonged heat stress. Increased area of stomatal pores, and higher chloroplast ultrastructure stability, were observed in primed plants, compared to non-primed plants at 45 °C. A total of 2049 and 882 differentially expressed genes (DEGs) were specifically identified in primed vs non-primed plants 6- and 12-h post stress application, respectively. These were associated with RNA degradation, ubiquitin mediated proteolysis, mRNA surveillance, glycerophospholipid metabolism and phosphatidylinositol signaling. These physiological and molecular mechanisms likely contributed to tomato resilience during heat stress. Acquired thermotolerance in tomatoes could therefore be mediated by enhanced ROS homeostasis and stomatal regulation, as well as higher structural stability of chloroplasts. Our study sheds new light on the physiological and molecular mechanisms underlying heat stress memory in tomato and provides valuable integrative transcriptomic-phenotypic datasets for this process.