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

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 tra...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 117; no. 1; pp. 741 - 751
Main Authors Nietzel, Thomas, Mostertz, Jörg, Ruberti, Cristina, Née, Guillaume, Fuchs, Philippe, Wagner, Stephan, Moseler, Anna, Müller-Schüssele, Stefanie J., Benamar, Abdelilah, Poschet, Gernot, Büttner, Michael, Møller, Ian Max, Lillig, Christopher H., Macherel, David, Wirtz, Markus, Hell, Rüdiger, Finkemeier, Iris, Meyer, Andreas J., Hochgräfe, Falko, Schwarzländer, Markus
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 07.01.2020
SeriesPNAS Plus
Subjects
Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.1910501117

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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.
AbstractList 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.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.
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.
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 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.
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.
Seeds are the main human food source and germination characteristics are critical in modern agriculture. For plants, seeds allow propagation over long distances and time periods and provide protection of progeny from hostile environments. For germination and seedling establishment the embryo relies fully on its stored energy resources. We report a sharp transition in mitochondrial metabolic activity and thiol redox status that coincides with seed rehydration. Hundreds of Cys-based redox switches are operated, providing early and direct metabolic regulation, long before gene expression-based control is established to underpin hormonal checkpoints. Seeds lacking proteins of the mitochondrial thiol redox machinery use their resources less efficiently, suggesting that the early reset of thiol redox status orchestrates metabolic efficiency for successful germination. 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.
Author Moseler, Anna
Büttner, Michael
Schwarzländer, Markus
Ruberti, Cristina
Benamar, Abdelilah
Müller-Schüssele, Stefanie J.
Hochgräfe, Falko
Wirtz, Markus
Meyer, Andreas J.
Finkemeier, Iris
Née, Guillaume
Poschet, Gernot
Wagner, Stephan
Mostertz, Jörg
Lillig, Christopher H.
Hell, Rüdiger
Macherel, David
Nietzel, Thomas
Fuchs, Philippe
Møller, Ian Max
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31871212$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Copyright National Academy of Sciences Jan 7, 2020
Distributed under a Creative Commons Attribution 4.0 International License
2020
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Issue 1
Keywords in vivo biosensing
redox regulation
seed germination
mitochondria
redox proteomics
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
Published under the PNAS license.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c477t-666b0d999694347cf6fb7237db4f4ff9faba3c0beeddf1a872beb8b01c74f44b3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
PMCID: PMC6955286
Edited by Bob B. Buchanan, University of California, Berkeley, CA, and approved November 20, 2019 (received for review June 19, 2019)
Author contributions: T.N., C.H.L., I.F., A.J.M., F.H., and M.S. designed research; T.N., J.M., C.R., G.N., P.F., A.B., G.P., M.B., D.M., and F.H. performed research; P.F., S.W., A.M., S.J.M.-S., R.H., I.F., and A.J.M. contributed new reagents/analytic tools; T.N., J.M., C.R., G.N., P.F., I.M.M., C.H.L., M.W., F.H., and M.S. analyzed data; and T.N. and M.S. wrote the paper.
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Snippet 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...
Seeds are the main human food source and germination characteristics are critical in modern agriculture. For plants, seeds allow propagation over long...
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SubjectTerms Activation
Adenosine Triphosphate - metabolism
Arabidopsis - physiology
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Biological Sciences
Biosensors
Citric Acid Cycle - physiology
Deregulation
Electron transport
Embryos
Energy metabolism
Energy storage
Fluorescence
Germination
Germination - physiology
Glutathione
Glutathione reductase
Glutathione Reductase - genetics
Glutathione Reductase - metabolism
Imbibition
Life Sciences
Metabolism
Mitochondria
Mitochondria - metabolism
NADP
Oxidation
Oxidation-Reduction
Oxygen - metabolism
Oxygen uptake
Peptides
Plants, Genetically Modified
PNAS Plus
Proteins
Proteomics
Proteomics - methods
Redox properties
Reductases
Resource efficiency
Respiration
Seed germination
Seeds
Seeds - cytology
Seeds - growth & development
Seeds - metabolism
Switches
Thioredoxin
Thioredoxin h - genetics
Thioredoxin h - metabolism
Thioredoxin-Disulfide Reductase - genetics
Thioredoxin-Disulfide Reductase - metabolism
Tricarboxylic acid cycle
Title Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination
URI https://www.jstor.org/stable/26897516
https://www.ncbi.nlm.nih.gov/pubmed/31871212
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https://pubmed.ncbi.nlm.nih.gov/PMC6955286
Volume 117
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