Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

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  • Thomas Nietzel, Institute of Plant Biology and Biotechnology, University of Münster, D-48143 Münster, Germany.
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  • Jörg Mostertz, Competence Center Functional Genomics, University of Greifswald, D-17489 Greifswald, Germany.
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  • Cristina Ruberti, Institute of Plant Biology and Biotechnology, University of Münster, D-48143 Münster, Germany.
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  • Guillaume Née, Institute of Plant Biology and Biotechnology, University of Münster, D-48143 Münster, Germany.
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  • Philippe Fuchs, Institute of Crop Science and Resource Conservation, University of Bonn, D-53113 Bonn, Germany.
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  • Stephan Wagner, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.
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  • Anna Moseler, Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de Lorraine, F-54506 Vandœuvre-lès-Nancy, France.
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  • Stefanie J Müller-Schüssele, Institute of Crop Science and Resource Conservation, University of Bonn, D-53113 Bonn, Germany.
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  • Abdelilah Benamar, Institut de Recherche en Horticulture et Semences, Université d'Angers, UMR 1345, F-49071 Beaucouzé Cedex, France.
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  • Gernot Poschet, Centre for Organismal Studies Heidelberg, Heidelberg University, D-69120 Heidelberg, Germany.
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  • Michael Büttner, Centre for Organismal Studies Heidelberg, Heidelberg University, D-69120 Heidelberg, Germany.
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  • Ian Max Møller
  • Christopher H Lillig, Institute for Medical Biochemistry and Molecular Biology, University Medicine Greifswald, D-17489 Greifswald, Germany.
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  • David Macherel, Institut de Recherche en Horticulture et Semences, Université d'Angers, UMR 1345, F-49071 Beaucouzé Cedex, France.
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  • Markus Wirtz, Centre for Organismal Studies Heidelberg, Heidelberg University, D-69120 Heidelberg, Germany.
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  • Rüdiger Hell, Centre for Organismal Studies Heidelberg, Heidelberg University, D-69120 Heidelberg, Germany.
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  • Iris Finkemeier, Institute of Plant Biology and Biotechnology, University of Münster, D-48143 Münster, Germany.
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  • Andreas J Meyer, Institute of Crop Science and Resource Conservation, University of Bonn, D-53113 Bonn, Germany.
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  • Falko Hochgräfe, Competence Center Functional Genomics, University of Greifswald, D-17489 Greifswald, Germany.
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  • Markus Schwarzländer, Institute of Plant Biology and Biotechnology, University of Münster, D-48143 Münster, Germany; markus.schwarzlander@uni-muenster.de.

Seeds preserve a far developed plant embryo in a quiescent state. Seed metabolism relies on stored resources and is reactivated to drive germination when the external conditions are favorable. Since the switchover from quiescence to reactivation provides a remarkable case of a cell physiological transition we investigated the earliest events in energy and redox metabolism of Arabidopsis seeds at imbibition. By developing fluorescent protein biosensing in intact seeds, we observed ATP accumulation and oxygen uptake within minutes, indicating rapid activation of mitochondrial respiration, which coincided with a sharp transition from an oxidizing to a more reducing thiol redox environment in the mitochondrial matrix. To identify individual operational protein thiol switches, we captured the fast release of metabolic quiescence in organello and devised quantitative iodoacetyl tandem mass tag (iodoTMT)-based thiol redox proteomics. The redox state across all Cys peptides was shifted toward reduction from 27.1% down to 13.0% oxidized thiol. A large number of Cys peptides (412) were redox switched, representing central pathways of mitochondrial energy metabolism, including the respiratory chain and each enzymatic step of the tricarboxylic acid (TCA) cycle. Active site Cys peptides of glutathione reductase 2, NADPH-thioredoxin reductase a/b, and thioredoxin-o1 showed the strongest responses. Germination of seeds lacking those redox proteins was associated with markedly enhanced respiration and deregulated TCA cycle dynamics suggesting decreased resource efficiency of energy metabolism. Germination in aged seeds was strongly impaired. We identify a global operation of thiol redox switches that is required for optimal usage of energy stores by the mitochondria to drive efficient germination.

Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue1
Pages (from-to)741-751
Number of pages11
ISSN0027-8424
DOIs
Publication statusPublished - 7 Jan 2020

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