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

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

Standard

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

I: Proceedings of the National Academy of Sciences of the United States of America, Bind 117, Nr. 1, 07.01.2020, s. 741-751.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

Harvard

Nietzel, T, Mostertz, J, Ruberti, C, Née, G, Fuchs, P, Wagner, S, Moseler, A, Müller-Schüssele, SJ, Benamar, A, Poschet, G, Büttner, M, Møller, IM, Lillig, CH, Macherel, D, Wirtz, M, Hell, R, Finkemeier, I, Meyer, AJ, Hochgräfe, F & Schwarzländer, M 2020, 'Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination', Proceedings of the National Academy of Sciences of the United States of America, bind 117, nr. 1, s. 741-751. https://doi.org/10.1073/pnas.1910501117

APA

Nietzel, T., Mostertz, J., Ruberti, C., Née, G., Fuchs, P., Wagner, S., Moseler, A., Müller-Schüssele, S. J., Benamar, A., Poschet, G., Büttner, M., Møller, I. M., Lillig, C. H., Macherel, D., Wirtz, M., Hell, R., Finkemeier, I., Meyer, A. J., Hochgräfe, F., & Schwarzländer, M. (2020). Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proceedings of the National Academy of Sciences of the United States of America, 117(1), 741-751. https://doi.org/10.1073/pnas.1910501117

CBE

Nietzel T, Mostertz J, Ruberti C, Née G, Fuchs P, Wagner S, Moseler A, Müller-Schüssele SJ, Benamar A, Poschet G, Büttner M, Møller IM, Lillig CH, Macherel D, Wirtz M, Hell R, Finkemeier I, Meyer AJ, Hochgräfe F, Schwarzländer M. 2020. Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proceedings of the National Academy of Sciences of the United States of America. 117(1):741-751. https://doi.org/10.1073/pnas.1910501117

MLA

Nietzel, Thomas o.a.. "Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination". Proceedings of the National Academy of Sciences of the United States of America. 2020, 117(1). 741-751. https://doi.org/10.1073/pnas.1910501117

Vancouver

Nietzel T, Mostertz J, Ruberti C, Née G, Fuchs P, Wagner S o.a. Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proceedings of the National Academy of Sciences of the United States of America. 2020 jan 7;117(1):741-751. https://doi.org/10.1073/pnas.1910501117

Author

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. / Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. I: Proceedings of the National Academy of Sciences of the United States of America. 2020 ; Bind 117, Nr. 1. s. 741-751.

Bibtex

@article{e8538c53fab641de8b18b75bbc3c1ae8,
title = "Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination",
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.",
author = "Thomas Nietzel and J{\"o}rg Mostertz and Cristina Ruberti and Guillaume N{\'e}e and Philippe Fuchs and Stephan Wagner and Anna Moseler and M{\"u}ller-Sch{\"u}ssele, {Stefanie J} and Abdelilah Benamar and Gernot Poschet and Michael B{\"u}ttner and M{\o}ller, {Ian Max} and Lillig, {Christopher H} and David Macherel and Markus Wirtz and R{\"u}diger Hell and Iris Finkemeier and Meyer, {Andreas J} and Falko Hochgr{\"a}fe and Markus Schwarzl{\"a}nder",
year = "2020",
month = jan,
day = "7",
doi = "10.1073/pnas.1910501117",
language = "English",
volume = "117",
pages = "741--751",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "1",

}

RIS

TY - JOUR

T1 - Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

AU - Nietzel, Thomas

AU - Mostertz, Jörg

AU - Ruberti, Cristina

AU - Née, Guillaume

AU - Fuchs, Philippe

AU - Wagner, Stephan

AU - Moseler, Anna

AU - Müller-Schüssele, Stefanie J

AU - Benamar, Abdelilah

AU - Poschet, Gernot

AU - Büttner, Michael

AU - Møller, Ian Max

AU - Lillig, Christopher H

AU - Macherel, David

AU - Wirtz, Markus

AU - Hell, Rüdiger

AU - Finkemeier, Iris

AU - Meyer, Andreas J

AU - Hochgräfe, Falko

AU - Schwarzländer, Markus

PY - 2020/1/7

Y1 - 2020/1/7

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.1910501117

DO - 10.1073/pnas.1910501117

M3 - Journal article

C2 - 31871212

VL - 117

SP - 741

EP - 751

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 1

ER -