Welcome Pathogens: Transient Heat Dampens Immune Responses to Acibenzolar-S-Methyl in Apple Plants

Climate change affects plant-pathogen interactions, with disease outcome varying depending on the pathosystem and environmental scenario. In Arabidopsis, a thermo-sensitive module of salicylic acid (SA) signalling makes immunity vulnerable to heat. The potent resistance inducer acibenzolar-S-methyl (ASM), an SA analogue that up-regulates transcription of defence genes, could restore plant protection under heat but not core SA signalling. Here, we investigated how high temperature rewires the ASM-induced responses of the apple immune system. We treated apple plants with ASM under contrasting heatwave scenarios and subsequently exposed them to Erwinia amylovora (the fire blight bacterium) or Venturia inaequalis (the apple scab fungus) while monitoring gene expression. While pre-exposing apple plants to high temperature did not change their susceptibility to pathogens, it drove a loss of ASM-induced protection. Transcriptomic analysis revealed broad dampening of ASM-regulation upon high temperature, for a wide range of biological processes beyond defence. We uncovered thermo-sensitive 'resistance' and 'susceptibility' marker genes with ASM-responsiveness being critically vulnerable to heat. We concluded that exposure to heatwaves prevents ASM from fully mounting its protective responses in apple, not only lowering defences but also offering more favourable hosting conditions. Our work highlights plant immunity as the joint outcome of resistant and susceptible responses.