title: Inactivation of Mitochondrial Complex I Induces the Expression of a Twin Cysteine Protein that Targets and Affects Cytosolic, Chloroplastidic and Mitochondrial Function.
abstract: At12Cys-1 (At5g64400) and At12Cys-2 (At5g09570) are two closely related isogenes that encode small, twin cysteine proteins, typically located in mitochondria. At12Cys-2 transcript is induced in a variety of mutants with disrupted mitochondrial proteins, but an increase in At12Cys protein is only detected in mutants with reduced mitochondrial complex I abundance. Induction of At12Cys protein in mutants that lack mitochondrial complex I is accompanied by At12Cys protein located in mitochondria, chloroplasts, and the cytosol. Biochemical analyses revealed that even single gene deletions, i.e., At12cys-1 or At12cys-2, have an effect on mitochondrial and chloroplast functions. However, only double mutants, i.e., At12cys-1:At12cys-2, affect the abundance of protein and mRNA transcripts encoding translation elongation factors as well as rRNA abundance. Blue native PAGE showed that At12Cys co-migrated with mitochondrial supercomplex I + III. Likewise, deletion of both At12cys-1 and At12cys-2 genes, but not single gene deletions, results in enhanced tolerance to drought and light stress and increased anti-oxidant capacity. The induction and multiple localization of At12Cys upon a reduction in complex I abundance provides a mechanism to specifically signal mitochondrial dysfunction to the cytosol and then beyond to other organelles in the cell.
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia.
authors.forename: Yan
authors.initials: Y
authors.lastname: Wang
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia.
authors.forename: Wenhui
authors.initials: W
authors.lastname: Lyu
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia.
authors.forename: Oliver
authors.initials: O
authors.lastname: Berkowitz
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia.
authors.forename: Jordan D
authors.initials: JD
authors.lastname: Radomiljac
authors.affiliation: Umeå Plant Science Centre (UPSC), Faculty of Science and Technology, Umeå University, Umeå, Sweden.
authors.forename: Simon R
authors.initials: SR
authors.lastname: Law
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
authors.forename: Monika W
authors.initials: MW
authors.lastname: Murcha
authors.affiliation: Department of Biology I, Botany, Ludwig-Maximilians-Universität München, Großhaderner Strasse 2-4, 82152 Planegg-Martinsried, Germany.
authors.forename: Chris
authors.initials: C
authors.lastname: Carrie
authors.affiliation: Department of Biochemistry and Biophysics, Stockholm University, Arrhenius Laboratories for Natural Sciences, 10691 Stockholm, Sweden.
authors.forename: Pedro F
authors.initials: PF
authors.lastname: Teixeira
authors.affiliation: Department of Biochemistry and Biophysics, Stockholm University, Arrhenius Laboratories for Natural Sciences, 10691 Stockholm, Sweden.
authors.forename: Beata
authors.initials: B
authors.lastname: Kmiec
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
authors.forename: Owen
authors.initials: O
authors.lastname: Duncan
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
authors.forename: Olivier
authors.initials: O
authors.lastname: Van Aken
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia.
authors.forename: Reena
authors.initials: R
authors.lastname: Narsai
authors.affiliation: Department of Biochemistry and Biophysics, Stockholm University, Arrhenius Laboratories for Natural Sciences, 10691 Stockholm, Sweden.
authors.forename: Elzbieta
authors.initials: E
authors.lastname: Glaser
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
authors.forename: Shaobai
authors.initials: S
authors.lastname: Huang
authors.affiliation: School of BioSciences, The University of Melbourne, Melbourne, VIC 3010, Australia.
authors.forename: Ute
authors.initials: U
authors.lastname: Roessner
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
authors.forename: A Harvey
authors.initials: AH
authors.lastname: Millar
authors.affiliation: Department of Animal, Plant and Soil Science, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, VIC 3086, Australia. Electronic address: j.whelan@latrobe.edu.au.
authors.forename: James
authors.initials: J
authors.lastname: Whelan
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism*; D003600:Cytosol / Q000378:metabolism; D042967:Electron Transport Complex I / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D008928:Mitochondria / Q000235:genetics / Q000378:metabolism*; D024101:Mitochondrial Proteins / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction
chemical_list: D029681:Arabidopsis Proteins; D024101:Mitochondrial Proteins; D042967:Electron Transport Complex I
keywords: chloroplast; complex I; cytosol; mitochondria; retrograde signaling