1. Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination
- Author
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Thomas Nietzel, Stephan Wagner, Gernot Poschet, Michael Büttner, Abdelilah Benamar, Anna Moseler, Ian M. Møller, Falko Hochgräfe, Rüdiger Hell, Iris Finkemeier, Stefanie J Müller-Schüssele, Markus Schwarzländer, Cristina Ruberti, Andreas J. Meyer, Guillaume Née, Markus Wirtz, Jörg Mostertz, David Macherel, Christopher Horst Lillig, Philippe Fuchs, Rheinische Friedrich-Wilhelms-Universität Bonn, General Electric Medical Systems [Buc] (GE Healthcare), General Electric Medical Systems, équipe RV&RA, Centre de Robotique (CAOR), MINES ParisTech - École nationale supérieure des mines de Paris-PSL Research University (PSL)-MINES ParisTech - École nationale supérieure des mines de Paris-PSL Research University (PSL), Department of Mathematical Sciences [Matieland, Stellenbosch Uni.] (DMS), Stellenbosch University, Institute of Crop Science and Resource Conservation (INRES), Institut de Recherche en Horticulture et Semences (IRHS), Université d'Angers (UA)-AGROCAMPUS OUEST-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Molekulkar Pflanzenphysiologie, Universität Erlangen-Nürnberg, AGROCAMPUS OUEST-Institut National de la Recherche Agronomique (INRA)-Université d'Angers (UA), Centre for Organismal Studies [Heidelberg] (COS), Heidelberg University, Plant Proteomics Group, Max Planck Institute for Plant Breeding Research (MPIPZ), Institut für Nutzpflanzenwissenschaften und Ressourcenschutz (INRES), Institut für Biologie und Biotechnologie der Pflanzen, University of Münster, Institute of Crop Science and Resource Conservation [Bonn] (INRES), Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université d'Angers (UA)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Friedrich-Alexander Universität Erlangen-Nürnberg (FAU), AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de la Recherche Agronomique (INRA)-Université d'Angers (UA), German Research Foundation (DFG) : SCHW1719/1-1, SPP1710 SCHW1719/7-1, ME1567/9-1/2, LI 984/3-1/2, INST 211/744-1, FUGG SCHW1719/5-1, and FI1655/3-1.
- Subjects
Proteomics ,0301 basic medicine ,0106 biological sciences ,Thioredoxin-Disulfide Reductase ,[SDV]Life Sciences [q-bio] ,Citric Acid Cycle ,Thioredoxin h ,Glutathione reductase ,Arabidopsis ,Respiratory chain ,seed germination ,Germination ,Reductase ,Mitochondrion ,01 natural sciences ,Redox ,redox regulation ,03 medical and health sciences ,Adenosine Triphosphate ,ComputingMilieux_MISCELLANEOUS ,030304 developmental biology ,2. Zero hunger ,chemistry.chemical_classification ,0303 health sciences ,Multidisciplinary ,Arabidopsis Proteins ,in vivo biosensing ,Chemistry ,Metabolism ,Plants, Genetically Modified ,redox proteomics ,Cell biology ,Oxygen ,mitochondria ,Citric acid cycle ,Glutathione Reductase ,030104 developmental biology ,Enzyme ,PNAS Plus ,Biochemistry ,Mitochondrial matrix ,Seeds ,Oxidation-Reduction ,010606 plant biology & botany - Abstract
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.
- Published
- 2020
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