Salicylic acid-dependent plant stress signalling via mitochondrial succinate dehydrogenase.
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Mitochondria are known for their role in ATP production and generation of reactive oxygen species (ROS), but little is known about the mechanism of their early involvement in plant stress signalling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signalling was analysed using two mutants; disrupted in stress response 1 (dsr1) which is a point mutation in SDH1 identified in a loss of SA signalling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type; while dsr1 also showed low succinate affinity, low catalytic efficiency and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterisation showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H2O2 production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H2O2 production in vitro in line with their low SA-dependent stress signalling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signalling by increased rates of mitochondrial H2O2 production, leading to part of the SA-dependent transcriptional response in plant cells.
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