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

Identifieur interne : 000093 ( Main/Exploration ); précédent : 000092; suivant : 000094

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

Auteurs : Alban Launay [France] ; Cécile Cabassa-Hourton [France] ; Holger Eubel [Allemagne] ; Régis Maldiney [France] ; Anne Guivarc'H [France] ; Emilie Crilat [France] ; Séverine Planchais [France] ; Jérôme Lacoste [France] ; Marianne Bordenave-Jacquemin [France] ; Gilles Clément [France] ; Luc Richard [France] ; Pierre Carol [France] ; Hans-Peter Braun [Allemagne] ; Sandrine Lebreton [France] ; Arnould Savouré [France]

Source :

RBID : pubmed:31504781

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English descriptors

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.

DOI: 10.1093/jxb/erz351
PubMed: 31504781
PubMed Central: PMC6859731


Affiliations:


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<term>Arabidopsis (metabolism)</term>
<term>Arabidopsis Proteins (chemistry)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Arabidopsis Proteins (metabolism)</term>
<term>Cell Respiration (MeSH)</term>
<term>Chlorophyll (metabolism)</term>
<term>Darkness (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Metabolome (MeSH)</term>
<term>Mitochondria (metabolism)</term>
<term>Mitochondria (ultrastructure)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Oxygen Consumption (MeSH)</term>
<term>Plant Leaves (growth & development)</term>
<term>Plant Leaves (metabolism)</term>
<term>Proline (metabolism)</term>
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<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (métabolisme)</term>
<term>Chlorophylle (métabolisme)</term>
<term>Consommation d'oxygène (MeSH)</term>
<term>Feuilles de plante (croissance et développement)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Mitochondries (métabolisme)</term>
<term>Mitochondries (ultrastructure)</term>
<term>Métabolome (MeSH)</term>
<term>Obscurité (MeSH)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Proline (métabolisme)</term>
<term>Protéines d'Arabidopsis (composition chimique)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines d'Arabidopsis (métabolisme)</term>
<term>Respiration cellulaire (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Séquence d'acides aminés (MeSH)</term>
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<term>Arabidopsis Proteins</term>
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<term>Feuilles de plante</term>
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<term>Arabidopsis</term>
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<term>Arabidopsis</term>
<term>Arabidopsis Proteins</term>
<term>Chlorophyll</term>
<term>Mitochondria</term>
<term>Plant Leaves</term>
<term>Proline</term>
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<term>Arabidopsis</term>
<term>Chlorophylle</term>
<term>Feuilles de plante</term>
<term>Mitochondries</term>
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<term>Mitochondria</term>
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<term>Amino Acid Sequence</term>
<term>Cell Respiration</term>
<term>Darkness</term>
<term>Gene Expression Regulation, Plant</term>
<term>Metabolome</term>
<term>Oxidation-Reduction</term>
<term>Oxygen Consumption</term>
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<term>Consommation d'oxygène</term>
<term>Mitochondries</term>
<term>Métabolome</term>
<term>Obscurité</term>
<term>Oxydoréduction</term>
<term>Respiration cellulaire</term>
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<div type="abstract" xml:lang="en">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.</div>
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<Issue>21</Issue>
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<AbstractText>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.</AbstractText>
<CopyrightInformation>© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.</CopyrightInformation>
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<ForeName>Alban</ForeName>
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<LastName>Cabassa-Hourton</LastName>
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