Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Alban Launay
  • Cécile Cabassa-Hourton
  • Holger Eubel
  • Régis Maldiney
  • Anne Guivarc'h
  • Emilie Crilat
  • Séverine Planchais
  • Jérôme Lacoste
  • Marianne Bordenave-Jacquemin
  • Gilles Clément
  • Luc Richard
  • Pierre Carol
  • Hans Peter Braun
  • Sandrine Lebreton
  • Arnould Savouré

Research Organisations

External Research Organisations

  • Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE)
  • Sorbonne Université
View graph of relations

Details

Original languageEnglish
Pages (from-to)6203-6214
Number of pages12
JournalJournal of experimental botany
Volume70
Issue number21
Early online date27 Aug 2019
Publication statusPublished - 1 Nov 2019

Abstract

Leaf senescence is a form of developmentally programmed cell death that allows the remobilization of nutrients and cellular materials from leaves to sink tissues and organs. Among the catabolic reactions that occur upon senescence, little is known about the role of proline catabolism. In this study, the involvement in dark-induced senescence of proline dehydrogenases (ProDHs), which catalyse the first and rate-limiting step of proline oxidation in mitochondria, was investigated using prodh single- and double-mutants with the help of biochemical, proteomic, and metabolomic approaches. The presence of ProDH2 in mitochondria was confirmed by mass spectrometry and immunogold labelling in dark-induced leaves of Arabidopsis. The prodh1 prodh2 mutant exhibited enhanced levels of most tricarboxylic acid cycle intermediates and free amino acids, demonstrating a role of ProDH in mitochondrial metabolism. We also found evidence of the involvement and the importance of ProDH in respiration, with proline as an alternative substrate, and in remobilization of proline during senescence to generate glutamate and energy that can then be exported to sink tissues and organs.

Keywords

    Arabidopsis thaliana, dark-induced leaf senescence, mitochondria, primary metabolism, proline dehydrogenase, proline metabolism, Amino Acid Sequence, Darkness, Proline/metabolism, Mitochondria/metabolism, Oxidation-Reduction, Chlorophyll/metabolism, Arabidopsis/genetics, Oxygen Consumption, Metabolome, Plant Leaves/growth & development, Cell Respiration, Gene Expression Regulation, Plant, Arabidopsis Proteins/chemistry

ASJC Scopus subject areas

Cite this

Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana. / Launay, Alban; Cabassa-Hourton, Cécile; Eubel, Holger et al.
In: Journal of experimental botany, Vol. 70, No. 21, 01.11.2019, p. 6203-6214.

Research output: Contribution to journalArticleResearchpeer review

Launay, A, Cabassa-Hourton, C, Eubel, H, Maldiney, R, Guivarc'h, A, Crilat, E, Planchais, S, Lacoste, J, Bordenave-Jacquemin, M, Clément, G, Richard, L, Carol, P, Braun, HP, Lebreton, S & Savouré, A 2019, 'Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana', Journal of experimental botany, vol. 70, no. 21, pp. 6203-6214. https://doi.org/10.1093/jxb/erz351
Launay, A., Cabassa-Hourton, C., Eubel, H., Maldiney, R., Guivarc'h, A., Crilat, E., Planchais, S., Lacoste, J., Bordenave-Jacquemin, M., Clément, G., Richard, L., Carol, P., Braun, H. P., Lebreton, S., & Savouré, A. (2019). Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana. Journal of experimental botany, 70(21), 6203-6214. https://doi.org/10.1093/jxb/erz351
Launay A, Cabassa-Hourton C, Eubel H, Maldiney R, Guivarc'h A, Crilat E et al. Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana. Journal of experimental botany. 2019 Nov 1;70(21):6203-6214. Epub 2019 Aug 27. doi: 10.1093/jxb/erz351
Download
@article{834c6941a6e943a29c1d6f986a063fb9,
title = "Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana",
abstract = "Leaf senescence is a form of developmentally programmed cell death that allows the remobilization of nutrients and cellular materials from leaves to sink tissues and organs. Among the catabolic reactions that occur upon senescence, little is known about the role of proline catabolism. In this study, the involvement in dark-induced senescence of proline dehydrogenases (ProDHs), which catalyse the first and rate-limiting step of proline oxidation in mitochondria, was investigated using prodh single- and double-mutants with the help of biochemical, proteomic, and metabolomic approaches. The presence of ProDH2 in mitochondria was confirmed by mass spectrometry and immunogold labelling in dark-induced leaves of Arabidopsis. The prodh1 prodh2 mutant exhibited enhanced levels of most tricarboxylic acid cycle intermediates and free amino acids, demonstrating a role of ProDH in mitochondrial metabolism. We also found evidence of the involvement and the importance of ProDH in respiration, with proline as an alternative substrate, and in remobilization of proline during senescence to generate glutamate and energy that can then be exported to sink tissues and organs.",
keywords = "Arabidopsis thaliana, dark-induced leaf senescence, mitochondria, primary metabolism, proline dehydrogenase, proline metabolism, Amino Acid Sequence, Darkness, Proline/metabolism, Mitochondria/metabolism, Oxidation-Reduction, Chlorophyll/metabolism, Arabidopsis/genetics, Oxygen Consumption, Metabolome, Plant Leaves/growth & development, Cell Respiration, Gene Expression Regulation, Plant, Arabidopsis Proteins/chemistry",
author = "Alban Launay and C{\'e}cile Cabassa-Hourton and Holger Eubel and R{\'e}gis Maldiney and Anne Guivarc'h and Emilie Crilat and S{\'e}verine Planchais and J{\'e}r{\^o}me Lacoste and Marianne Bordenave-Jacquemin and Gilles Cl{\'e}ment and Luc Richard and Pierre Carol and Braun, {Hans Peter} and Sandrine Lebreton and Arnould Savour{\'e}",
note = "Funding information: We are indebted to Dr Dietmar Funck for kindly providing an antibody directed against P5CDH.We thank the electron microscopy team of the IBPS Imaging Facility, Sorbonne University for their help with the experiments. This study received financial support from Sorbonne University.",
year = "2019",
month = nov,
day = "1",
doi = "10.1093/jxb/erz351",
language = "English",
volume = "70",
pages = "6203--6214",
journal = "Journal of experimental botany",
issn = "0022-0957",
publisher = "Oxford University Press",
number = "21",

}

Download

TY - JOUR

T1 - Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana

AU - Launay, Alban

AU - Cabassa-Hourton, Cécile

AU - Eubel, Holger

AU - Maldiney, Régis

AU - Guivarc'h, Anne

AU - Crilat, Emilie

AU - Planchais, Séverine

AU - Lacoste, Jérôme

AU - Bordenave-Jacquemin, Marianne

AU - Clément, Gilles

AU - Richard, Luc

AU - Carol, Pierre

AU - Braun, Hans Peter

AU - Lebreton, Sandrine

AU - Savouré, Arnould

N1 - Funding information: We are indebted to Dr Dietmar Funck for kindly providing an antibody directed against P5CDH.We thank the electron microscopy team of the IBPS Imaging Facility, Sorbonne University for their help with the experiments. This study received financial support from Sorbonne University.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - Leaf senescence is a form of developmentally programmed cell death that allows the remobilization of nutrients and cellular materials from leaves to sink tissues and organs. Among the catabolic reactions that occur upon senescence, little is known about the role of proline catabolism. In this study, the involvement in dark-induced senescence of proline dehydrogenases (ProDHs), which catalyse the first and rate-limiting step of proline oxidation in mitochondria, was investigated using prodh single- and double-mutants with the help of biochemical, proteomic, and metabolomic approaches. The presence of ProDH2 in mitochondria was confirmed by mass spectrometry and immunogold labelling in dark-induced leaves of Arabidopsis. The prodh1 prodh2 mutant exhibited enhanced levels of most tricarboxylic acid cycle intermediates and free amino acids, demonstrating a role of ProDH in mitochondrial metabolism. We also found evidence of the involvement and the importance of ProDH in respiration, with proline as an alternative substrate, and in remobilization of proline during senescence to generate glutamate and energy that can then be exported to sink tissues and organs.

AB - Leaf senescence is a form of developmentally programmed cell death that allows the remobilization of nutrients and cellular materials from leaves to sink tissues and organs. Among the catabolic reactions that occur upon senescence, little is known about the role of proline catabolism. In this study, the involvement in dark-induced senescence of proline dehydrogenases (ProDHs), which catalyse the first and rate-limiting step of proline oxidation in mitochondria, was investigated using prodh single- and double-mutants with the help of biochemical, proteomic, and metabolomic approaches. The presence of ProDH2 in mitochondria was confirmed by mass spectrometry and immunogold labelling in dark-induced leaves of Arabidopsis. The prodh1 prodh2 mutant exhibited enhanced levels of most tricarboxylic acid cycle intermediates and free amino acids, demonstrating a role of ProDH in mitochondrial metabolism. We also found evidence of the involvement and the importance of ProDH in respiration, with proline as an alternative substrate, and in remobilization of proline during senescence to generate glutamate and energy that can then be exported to sink tissues and organs.

KW - Arabidopsis thaliana

KW - dark-induced leaf senescence

KW - mitochondria

KW - primary metabolism

KW - proline dehydrogenase

KW - proline metabolism

KW - Amino Acid Sequence

KW - Darkness

KW - Proline/metabolism

KW - Mitochondria/metabolism

KW - Oxidation-Reduction

KW - Chlorophyll/metabolism

KW - Arabidopsis/genetics

KW - Oxygen Consumption

KW - Metabolome

KW - Plant Leaves/growth & development

KW - Cell Respiration

KW - Gene Expression Regulation, Plant

KW - Arabidopsis Proteins/chemistry

UR - http://www.scopus.com/inward/record.url?scp=85075108185&partnerID=8YFLogxK

U2 - 10.1093/jxb/erz351

DO - 10.1093/jxb/erz351

M3 - Article

C2 - 31504781

AN - SCOPUS:85075108185

VL - 70

SP - 6203

EP - 6214

JO - Journal of experimental botany

JF - Journal of experimental botany

SN - 0022-0957

IS - 21

ER -

By the same author(s)