Thermotolerance is improved by heat stress (HS) acclimation, and the thermotolerance level is "remembered" by plants. However, the underlying signalling mechanisms remain largely unknown. Here, we showed NADPH oxidase-mediated H2 O2 (NADPH-H2 O2 ), and chloroplast-H2 O2 promoted the sustained expression of HS-responsive genes and programmed cell death (PCD) genes, respectively, during recovery after HS acclimation. When spraying the NADPH oxidase inhibitor, diphenylene iodonium, after HS acclimation, the NADPH-H2 O2 level significantly decreased, resulting in a decrease in the expression of HS-responsive genes and the loss of maintenance of acquired thermotolerance (MAT). In contrast, compared with HS acclimation, NADPH-H2 O2 declined but chloroplast-H2 O2 further enhanced during recovery after HS over-acclimation, resulting in the reduced expression of HS-responsive genes and substantial production of PCD. Notably, the further inhibition of NADPH-H2 O2 after HS over-acclimation also inhibited chloroplast-H2 O2 , alleviating the severe PCD and surpassing the MAT of HS over-acclimation treatment. Due to the change in subcellular H2 O2 after HS acclimation, the tomato seedlings maintained a constant H2 O2 level during recovery, resulting in stable and lower total H2 O2 levels during a tester HS challenge conducted after recovery. We conclude that tomato seedlings increase their MAT by enhancing NADPH-H2 O2 content and controlling chloroplast-H2 O2 production during recovery, which enhances the expression of HS-responsive genes and balances PCD levels, respectively.
Keywords: heat stress memory; tomato.
© 2018 John Wiley & Sons Ltd.