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

authored by

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

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.

Organisation(s)

Institute of Plant Genetics

External Organisation(s)

Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE)
Sorbonne Université

Type

Article

Journal

Journal of experimental botany

Volume

70

Pages

6203-6214

No. of pages

12

ISSN

0022-0957

Publication date

01.11.2019

Publication status

Published

Peer reviewed

Yes

ASJC Scopus subject areas

Physiology, Plant Science

Electronic version(s)

https://doi.org/10.1093/jxb/erz351 (Access: Open)