Dissecting the Metabolic Role of Mitochondria during Developmental Leaf Senescence.
Identifieur interne : 003D14 ( Ncbi/Merge ); précédent : 003D13; suivant : 003D15Dissecting the Metabolic Role of Mitochondria during Developmental Leaf Senescence.
Auteurs : Daria Chrobok ; Simon R. Law ; Bastiaan Brouwer ; Pernilla Lindén ; Agnieszka Ziolkowska ; Daniela Liebsch ; Reena Narsai ; Bozena Szal ; Thomas Moritz ; Nicolas Rouhier ; James Whelan ; Per Gardeström ; Olivier Keech [Suède]Source :
- Plant physiology [ 1532-2548 ] ; 2016.
Descripteurs français
- KwdFr :
- Analyse de profil d'expression de gènes, Arabidopsis (croissance et développement), Arabidopsis (génétique), Arabidopsis (métabolisme), Feuilles de plante (croissance et développement), Feuilles de plante (métabolisme), Feuilles de plante (ultrastructure), Gènes de mitochondrie, Gènes de plante, Mitochondries (métabolisme), Mitochondries (ultrastructure), Métabolisme énergétique, Métabolomique, Protéines mitochondriales (métabolisme), Respiration cellulaire, Régulation de l'expression des gènes végétaux, Transcription génétique, Transcriptome (génétique), Voies et réseaux métaboliques (génétique).
- MESH :
- croissance et développement : Arabidopsis, Feuilles de plante.
- génétique : Arabidopsis, Transcriptome, Voies et réseaux métaboliques.
- métabolisme : Arabidopsis, Feuilles de plante, Mitochondries, Protéines mitochondriales.
- ultrastructure : Analyse de profil d'expression de gènes, Feuilles de plante, Gènes de mitochondrie, Gènes de plante, Mitochondries, Métabolisme énergétique, Métabolomique, Respiration cellulaire, Régulation de l'expression des gènes végétaux, Transcription génétique.
English descriptors
- KwdEn :
- Arabidopsis (genetics), Arabidopsis (growth & development), Arabidopsis (metabolism), Cell Respiration, Energy Metabolism, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Mitochondrial, Genes, Plant, Metabolic Networks and Pathways (genetics), Metabolomics, Mitochondria (metabolism), Mitochondria (ultrastructure), Mitochondrial Proteins (metabolism), Plant Leaves (growth & development), Plant Leaves (metabolism), Plant Leaves (ultrastructure), Transcription, Genetic, Transcriptome (genetics).
- MESH :
- chemical , metabolism : Mitochondrial Proteins.
- genetics : Arabidopsis, Metabolic Networks and Pathways, Transcriptome.
- growth & development : Arabidopsis, Plant Leaves.
- metabolism : Arabidopsis, Mitochondria, Plant Leaves.
- ultrastructure : Mitochondria, Plant Leaves.
- Cell Respiration, Energy Metabolism, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Mitochondrial, Genes, Plant, Metabolomics, Transcription, Genetic.
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.
DOI: 10.1104/pp.16.01463
PubMed: 27744300
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pubmed:27744300Le document en format XML
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<front><div type="abstract" xml:lang="en">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.</div>
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<Abstract><AbstractText>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.</AbstractText>
<CopyrightInformation>© 2016 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chrobok</LastName>
<ForeName>Daria</ForeName>
<Initials>D</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-4842-7690</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Law</LastName>
<ForeName>Simon R</ForeName>
<Initials>SR</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-0389-6650</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Brouwer</LastName>
<ForeName>Bastiaan</ForeName>
<Initials>B</Initials>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lindén</LastName>
<ForeName>Pernilla</ForeName>
<Initials>P</Initials>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ziolkowska</LastName>
<ForeName>Agnieszka</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-4262-7106</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Liebsch</LastName>
<ForeName>Daniela</ForeName>
<Initials>D</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-2457-7376</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Narsai</LastName>
<ForeName>Reena</ForeName>
<Initials>R</Initials>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Szal</LastName>
<ForeName>Bozena</ForeName>
<Initials>B</Initials>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Moritz</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-4258-3190</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Rouhier</LastName>
<ForeName>Nicolas</ForeName>
<Initials>N</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2036-7884</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Whelan</LastName>
<ForeName>James</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5754-025X</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Gardeström</LastName>
<ForeName>Per</ForeName>
<Initials>P</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5900-7395</Identifier>
<AffiliationInfo><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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, S-90183 Umea, Sweden (P.L., T.M.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Institute of Experimental Plant Biology and Biotechnology, Faculty of Biology, University of Warsaw I, 02-096 Warsaw, Poland (B.S.); and.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Keech</LastName>
<ForeName>Olivier</ForeName>
<Initials>O</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-0546-7721</Identifier>
<AffiliationInfo><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.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>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.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2016</Year>
<Month>10</Month>
<Day>15</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>Plant Physiol</MedlineTA>
<NlmUniqueID>0401224</NlmUniqueID>
<ISSNLinking>0032-0889</ISSNLinking>
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