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Metabolic control of arginine and ornithine levels paces the progression of leaf senescence

Liebsch, Daniela and Juvany, Marta and Li, Zhonghai and Wang, Hou-Ling and Ziolkowska, Agnieszka and Chrobok, Daria and Boussardon, Clement and Wen, Xing and Law, Simon R. and Janeckova, Helena and Brouwer, Bastiaan and Linden, Pernilla and Delhomme, Nicolas and Stenlund, Hans and Moritz, Thomas and Gardestrom, Per and Guo, Hongwei and Keech, Olivier (2022). Metabolic control of arginine and ornithine levels paces the progression of leaf senescence. Plant Physiology
[Research article]

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Abstract

Pools of arginine and ornithine generated during protein degradation can pace the progression of leaf senescence by affecting the TCA cycle, polyamine biosynthesis and the ethylene signaling pathway.Leaf senescence can be induced by stress or aging, sometimes in a synergistic manner. It is generally acknowledged that the ability to withstand senescence-inducing conditions can provide plants with stress resilience. Although the signaling and transcriptional networks responsible for a delayed senescence phenotype, often referred to as a functional stay-green trait, have been actively investigated, very little is known about the subsequent metabolic adjustments conferring this aptitude to survival. First, using the individually darkened leaf (IDL) experimental setup, we compared IDLs of wild-type (WT) Arabidopsis (Arabidopsis thaliana) to several stay-green contexts, that is IDLs of two functional stay-green mutant lines, oresara1-2 (ore1-2) and an allele of phytochrome-interacting factor 5 (pif5), as well as to leaves from a WT plant entirely darkened (DP). We provide compelling evidence that arginine and ornithine, which accumulate in all stay-green contexts-likely due to the lack of induction of amino acids (AAs) transport-can delay the progression of senescence by fueling the Krebs cycle or the production of polyamines (PAs). Secondly, we show that the conversion of putrescine to spermidine (SPD) is controlled in an age-dependent manner. Thirdly, we demonstrate that SPD represses senescence via interference with ethylene signaling by stabilizing the ETHYLENE BINDING FACTOR1 and 2 (EBF1/2) complex. Taken together, our results identify arginine and ornithine as central metabolites influencing the stress- and age-dependent progression of leaf senescence. We propose that the regulatory loop between the pace of the AA export and the progression of leaf senescence provides the plant with a mechanism to fine-tune the induction of cell death in leaves, which, if triggered unnecessarily, can impede nutrient remobilization and thus plant growth and survival.

Authors/Creators:Liebsch, Daniela and Juvany, Marta and Li, Zhonghai and Wang, Hou-Ling and Ziolkowska, Agnieszka and Chrobok, Daria and Boussardon, Clement and Wen, Xing and Law, Simon R. and Janeckova, Helena and Brouwer, Bastiaan and Linden, Pernilla and Delhomme, Nicolas and Stenlund, Hans and Moritz, Thomas and Gardestrom, Per and Guo, Hongwei and Keech, Olivier
Title:Metabolic control of arginine and ornithine levels paces the progression of leaf senescence
Series Name/Journal:Plant Physiology
Year of publishing :2022
Number of Pages:18
Publisher:OXFORD UNIV PRESS INC
ISSN:0032-0889
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution-Noncommercial-No Derivative Works 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Botany
URN:NBN:urn:nbn:se:slu:epsilon-p-117571
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-117571
Additional ID:
Type of IDID
DOI10.1093/plphys/kiac244
Web of Science (WoS)000803838800001
ID Code:28572
Faculty:S - Faculty of Forest Sciences
Department:(S) > Dept. of Forest Genetics and Plant Physiology
Deposited By: SLUpub Connector
Deposited On:26 Aug 2022 08:12
Metadata Last Modified:26 Aug 2022 08:21

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