title: Dissecting the Metabolic Role of Mitochondria during Developmental Leaf Senescence.
abstract: The functions of mitochondria during leaf senescence, a type of programmed cell death aimed at the massive retrieval of nutrients from the senescing organ to the rest of the plant, remain elusive. Here, combining experimental and analytical approaches, we showed that mitochondrial integrity in Arabidopsis (Arabidopsis thaliana) is conserved until the latest stages of leaf senescence, while their number drops by 30%. Adenylate phosphorylation state assays and mitochondrial respiratory measurements indicated that the leaf energy status also is maintained during this time period. Furthermore, after establishing a curated list of genes coding for products targeted to mitochondria, we analyzed in isolation their transcript profiles, focusing on several key mitochondrial functions, such as the tricarboxylic acid cycle, mitochondrial electron transfer chain, iron-sulfur cluster biosynthesis, transporters, as well as catabolic pathways. In tandem with a metabolomic approach, our data indicated that mitochondrial metabolism was reorganized to support the selective catabolism of both amino acids and fatty acids. Such adjustments would ensure the replenishment of α-ketoglutarate and glutamate, which provide the carbon backbones for nitrogen remobilization. Glutamate, being the substrate of the strongly up-regulated cytosolic glutamine synthase, is likely to become a metabolically limiting factor in the latest stages of developmental leaf senescence. Finally, an evolutionary age analysis revealed that, while branched-chain amino acid and proline catabolism are very old mitochondrial functions particularly enriched at the latest stages of leaf senescence, auxin metabolism appears to be rather newly acquired. In summation, our work shows that, during developmental leaf senescence, mitochondria orchestrate catabolic processes by becoming increasingly central energy and metabolic hubs.
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Daria
authors.identifier: 0000-0002-4842-7690
authors.initials: D
authors.lastname: Chrobok
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Simon R
authors.identifier: 0000-0003-0389-6650
authors.initials: SR
authors.lastname: Law
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Bastiaan
authors.initials: B
authors.lastname: Brouwer
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Pernilla
authors.initials: P
authors.lastname: Lindén
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Agnieszka
authors.identifier: 0000-0002-4262-7106
authors.initials: A
authors.lastname: Ziolkowska
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Daniela
authors.identifier: 0000-0003-2457-7376
authors.initials: D
authors.lastname: Liebsch
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Reena
authors.initials: R
authors.lastname: Narsai
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Bozena
authors.initials: B
authors.lastname: Szal
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Thomas
authors.identifier: 0000-0002-4258-3190
authors.initials: T
authors.lastname: Moritz
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Nicolas
authors.identifier: 0000-0002-2036-7884
authors.initials: N
authors.lastname: Rouhier
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: James
authors.identifier: 0000-0001-5754-025X
authors.initials: J
authors.lastname: Whelan
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.).|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.).|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.).
authors.forename: Per
authors.identifier: 0000-0001-5900-7395
authors.initials: P
authors.lastname: Gardeström
authors.affiliation: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden (D.C., S.R.L., B.B., A.Z., D.L., P.G., O.K.); olivier.keech@umu.se.|Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.); olivier.keech@umu.se.|Department of Animal, Plant, and Soil Science, School of Life Science, Australian Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., J.W.); olivier.keech@umu.se.|Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and olivier.keech@umu.se.|Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Université de Lorraine/Institut National de la Recherche Agronomique Faculté des Sciences et Technologies, 54506 Vandoeuvre-les-Nancy, France (N.R.) olivier.keech@umu.se.
authors.forename: Olivier
authors.identifier: 0000-0002-0546-7721
authors.initials: O
authors.lastname: Keech
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism*; D019069:Cell Respiration; D004734:Energy Metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D050259:Genes, Mitochondrial; D017343:Genes, Plant; D053858:Metabolic Networks and Pathways / Q000235:genetics; D055432:Metabolomics; D008928:Mitochondria / Q000378:metabolism* / Q000648:ultrastructure; D024101:Mitochondrial Proteins / Q000378:metabolism; D018515:Plant Leaves / Q000254:growth & development* / Q000378:metabolism* / Q000648:ultrastructure; D014158:Transcription, Genetic; D059467:Transcriptome / Q000235:genetics
chemical_list: D024101:Mitochondrial Proteins