title: Mitochondrial and Chloroplast Stress Responses Are Modulated in Distinct Touch and Chemical Inhibition Phases.
abstract: Previous studies have identified a range of transcription factors that modulate retrograde regulation of mitochondrial and chloroplast functions in Arabidopsis (Arabidopsis thaliana). However, the relative importance of these regulators and whether they act downstream of separate or overlapping signaling cascades is still unclear. Here, we demonstrate that multiple stress-related signaling pathways, with distinct kinetic signatures, converge on overlapping gene sets involved in energy organelle function. The transcription factor ANAC017 is almost solely responsible for transcript induction of marker genes around 3 to 6 h after chemical inhibition of organelle function and is a key regulator of mitochondrial and specific types of chloroplast retrograde signaling. However, an independent and highly transient gene expression phase, initiated within 10 to 30 min after treatment, also targets energy organelle functions, and is related to touch and wounding responses. Metabolite analysis demonstrates that this early response is concurrent with rapid changes in tricarboxylic acid cycle intermediates and large changes in transcript abundance of genes encoding mitochondrial dicarboxylate carrier proteins. It was further demonstrated that transcription factors AtWRKY15 and AtWRKY40 have repressive regulatory roles in this touch-responsive gene expression. Together, our results show that several regulatory systems can independently affect energy organelle function in response to stress, providing different means to exert operational control.
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.) olivier.van.aken@uwa.edu.au.
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, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: Inge
authors.identifier: 0000-0001-8125-1239
authors.initials: I
authors.lastname: De Clercq
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: Aneta
authors.initials: A
authors.lastname: Ivanova
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: Simon R
authors.identifier: 0000-0003-0389-6650
authors.initials: SR
authors.lastname: Law
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: Frank
authors.identifier: 0000-0002-3147-0860
authors.initials: F
authors.lastname: Van Breusegem
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: A Harvey
authors.initials: AH
authors.lastname: Millar
authors.affiliation: ARC Centre of Excellence in Plant Energy Biology, Faculty of Science, The University of Western Australia, Crawley 6009, Western Australia, Australia (O.V.A., A.I., A.H.M.);Department of Botany, ARC Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia (I.D.C., S.R.L.);Department of Plant Systems Biology, VIB, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (I.D.C., F.V.B.); andDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umeå, Sweden (S.R.L.).
authors.forename: James
authors.initials: J
authors.lastname: Whelan
mesh_terms: D000968:Antimycin A / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D002736:Chloroplasts / Q000187:drug effects / Q000502:physiology*; D004734:Energy Metabolism / Q000235:genetics; D005463:Fluoroacetates / Q000494:pharmacology; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D008928:Mitochondria / Q000187:drug effects / Q000502:physiology*; D024101:Mitochondrial Proteins / Q000235:genetics; D030821:Plants, Genetically Modified; D015398:Signal Transduction / Q000187:drug effects; D013312:Stress, Physiological / Q000502:physiology*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: C000597111:ANAC017 protein, Arabidopsis; D029681:Arabidopsis Proteins; D005463:Fluoroacetates; D024101:Mitochondrial Proteins; C000607130:OM66 protein, Arabidopsis; D014157:Transcription Factors; C578017:WRKY15 protein, Arabidopsis; C512070:WRKY40 protein, Arabidopsis; D000968:Antimycin A; C014815:fluoroacetic acid