Details
| Original language | English |
|---|---|
| Pages (from-to) | 6203-6214 |
| Number of pages | 12 |
| Journal | Journal of experimental botany |
| Volume | 70 |
| Issue number | 21 |
| Early online date | 27 Aug 2019 |
| Publication status | Published - 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
- Biochemistry, Genetics and Molecular Biology(all)
- Physiology
- Agricultural and Biological Sciences(all)
- Plant Science
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In: Journal of experimental botany, Vol. 70, No. 21, 01.11.2019, p. 6203-6214.
Research output: Contribution to journal › Article › Research › peer review
}
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 -