title: Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase.
abstract: Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants:disrupted in stress response1(dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling 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, whiledsr1also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued insdhaf2, but not indsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H2O2production. Bothdsr1andsdhaf2showed lower rates of SA-dependent H2O2production in vitro in line with their low SA-dependent stress signaling 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 signaling by increased rates of mitochondrial H2O2production, leading to part of the SA-dependent transcriptional response in plant cells.
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Katharina
authors.identifier: 0000-0002-3142-5656
authors.initials: K
authors.lastname: Belt
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Shaobai
authors.identifier: 0000-0003-3667-611X
authors.initials: S
authors.lastname: Huang
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Louise F
authors.initials: LF
authors.lastname: Thatcher
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Hayley
authors.identifier: 0000-0003-2399-0599
authors.initials: H
authors.lastname: Casarotto
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Karam B
authors.identifier: 0000-0002-2777-7448
authors.initials: KB
authors.lastname: Singh
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: Olivier
authors.identifier: 0000-0003-4024-968X
authors.initials: O
authors.lastname: Van Aken
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, Bayliss Building M316, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia (K.B., S.H., O.V.A., A.H.M.).|Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, Wembley, Washington 6913, Australia (L.F.T., H.C., K.B.S.); and.|University of Western Australia Institute of Agriculture, University of Western Australia, Crawley, Washington 6009, Australia (K.B.S.).
authors.forename: A Harvey
authors.identifier: 0000-0001-9679-1473
authors.initials: AH
authors.lastname: Millar
mesh_terms: D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D006861:Hydrogen Peroxide / Q000378:metabolism; D007700:Kinetics; D008928:Mitochondria / Q000187:drug effects / Q000201:enzymology* / Q000378:metabolism; D009154:Mutation; D010101:Oxygen Consumption / Q000187:drug effects; D030821:Plants, Genetically Modified; D011401:Promoter Regions, Genetic / Q000235:genetics; D017382:Reactive Oxygen Species / Q000378:metabolism; D020156:Salicylic Acid / Q000378:metabolism* / Q000494:pharmacology; D015398:Signal Transduction; D013312:Stress, Physiological; D013385:Succinate Dehydrogenase / Q000235:genetics / Q000378:metabolism*; D019802:Succinic Acid / Q000378:metabolism; D014451:Ubiquinone / Q000378:metabolism
chemical_list: D017382:Reactive Oxygen Species; D014451:Ubiquinone; D019802:Succinic Acid; D006861:Hydrogen Peroxide; D013385:Succinate Dehydrogenase; D020156:Salicylic Acid