Dataset Information

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.

SUBMITTER: Launay A

PROVIDER: S-EPMC6859731 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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

Launay Alban A Cabassa-Hourton Cécile C Eubel Holger H Maldiney Régis R Guivarc'h Anne A Crilat Emilie E Planchais Séverine S Lacoste Jérôme J Bordenave-Jacquemin Marianne M Clément Gilles G Richard Luc L Carol Pierre P Braun Hans-Peter HP Lebreton Sandrine S Savouré Arnould A

Journal of experimental botany 20191101 21

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 singl ...[more]

PMID: 31504781

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Project description:The aim of this study was to gain insight into the compartment-specific roles of ascorbate and glutathione in leaf senescence in Arabidopsis thaliana. The subcellular distribution of ascorbate, glutathione, and hydrogen peroxide (H2O2) was analyzed by transmission electron microscopy and correlated with the activity of antioxidative enzymes in wildtype plants and the ascorbate- and glutathione-deficient mutants vtc2-1 and pad2-1, respectively. Both mutants showed earlier and stronger senescence than the wildtype indicating the importance of a functioning ascorbate and glutathione cycle in the induction and regulation of senescence. Glutathione levels dropped drastically and up to 93 % in all cell compartments of wildtype plants and the vtc2-1 mutant within the first day of dark-induced senescence while ascorbate contents remained unchanged until the very end. Glutathione contents in mitochondria of pad2-1 mutants decreased more slowly over the first 7 days than compared to the other plants indicating an important role of glutathione in mitochondria in this mutant during senescence. The strongest decrease (84 %) of glutathione contents in wildtype plants at this time point was found in mitochondria indicating an important role of mitochondria for the induction of senescence and cell death events. Due to the general decrease of the antioxidative capacity, a strong accumulation of H2O2 was observed in cell walls, plastids, and the cytosol in all plants. Activities of glutathione reductase, dehydroascorbate reductase and catalase were strongly reduced while ascorbate peroxidase and monodehydroascorbate reductase were increased. The initial rapid drop of glutathione levels seemed to be the trigger for senescence, while ascorbate appeared to be the key factor in regulating senescence through controlling H2O2 levels by the oxidation of reduced ascorbate to monodehydroascorbate and the subsequent reduction to ascorbate by monodehydroascorbate reductase.

Dataset Information

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

Publications

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

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