Tomato miR398 knockout disrupts ROS dynamics during stress conferring heat tolerance but hypersusceptibility to necrotroph infection.

Abstract

An imbalance between ROS production and scavenging during stress results in oxidative bursts, which causes cellular damage. miR398 is a regulator of ROS scavenging since it targets crucial Cu/Zn superoxide dismutases (CSDs). Established functional studies aligned miR398 with plants' heat and heavy metal stress fitness. However, a knowledge gap in the dynamics of miR398-CSD interaction for redox regulation during pathogenic development impeded their use in crop improvement programmes. We use tomato, Solanum lycopersicum, plants, and necrotrophic and biotrophic pathogens to show that a complex transcriptional and post-transcriptional regulatory circuit maintains SlmiR398 and its target SlCSD genes' level. The interaction is indispensable for ROS regulation in either the pathogenic outcome, thermal stress, or a combination of both stresses, as observed in the cultivation field. The SlmiR398 knockout plants display feeble O2^∙- accumulation but enhanced levels of H₂O₂, several defense-related genes, metabolites, and vital HSFs and HSPs, which were heightened upon stress. Depletion of SlmiR398, although it renders thermotolerance and resilience to biotrophic pathogens likely due to the augmented hypersensitive response, facilitates necrotrophy. Thus, SlmiR398-mediated ROS regulation seemingly works at the interface of abiotic and biotic stress response for a sustainable reaction of tomato plants.