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)