Primary metabolism determines the outcome of salicylic acid-mediated immune induction

Abstract

Controlling the deleterious effects of immune responses is as vital as fighting infection. In plants, this is achieved, in part, by circadian clock-mediated regulation, such as the synthesis of and response to the immune hormone salicylic acid (SA)1,2. Application of SA at the same concentration under light/dark cycles induces immunity with minimal impact on growth, however, prolonged darkness leads to plant death2. To uncover what determines this life-or-death outcome, we identified twenty survival of SA-induced death (ssd) mutants through genetic screening. These mutants are defective in starch, glucose, and nitrate metabolism, and circadian regulation, and accumulate excessive starch and/or glucose. Likewise, glucose application rescues SA-treated plants in prolonged darkness. Surprisingly, SA treatment does not deplete glucose, but instead, induces amino acid and fatty acid catabolism. Through transcriptomic analyses of glucose-rescued WT plants and ssd mutants for shared pathways, we found that SA triggers plant death in darkness by inducing oxidative stress, and water loss, while glucose antagonizes these processes, boosts ER protein processing and re-establishes the anabolism-catabolism balance. Interestingly, the programmed cell death induced by effector-triggered immunity shares common transcriptomic patterns with those observed during SA-induced cell death in darkness and could also be attenuated by glucose treatment. Therefore, coordination with the cellular metabolic context plays a central role in determining immune outcomes and optimizing plant health.