Research article - Peer-reviewed, 2022
Metabolic control of arginine and ornithine levels paces the progression of leaf senescence
Liebsch, Daniela; Juvany, Marta; Li, Zhonghai; Wang, Hou-Ling; Ziolkowska, Agnieszka; Chrobok, Daria; Boussardon, Clement; Wen, Xing; Law, Simon R.; Janeckova, Helena; Brouwer, Bastiaan; Linden, Pernilla; Delhomme, Nicolas; Stenlund, Hans; Moritz, Thomas; Gardestrom, Per; Guo, Hongwei; Keech, OlivierAbstract
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.Published in
Plant Physiology2022,
Publisher: OXFORD UNIV PRESS INC
Authors' information
Liebsch, Daniela
Umea University
Juvany, Marta
Umea University
Li, Zhonghai
Beijing Forestry University
Wang, Hou-Ling
Beijing Forestry University
Ziolkowska, Agnieszka
Umea University
Chrobok, Daria
Umea University
Boussardon, Clement
Umea University
Wen, Xing
Southern University of Science and Technology
Law, Simon R.
Umea University
Janeckova, Helena
Palacky University Olomouc
Brouwer, Bastiaan
Umea University
Linden, Pernilla
Umea University
Umea University
Swedish University of Agricultural Sciences, Department of Forest Genetics and Plant Physiology
Umea University
Swedish University of Agricultural Sciences, Department of Forest Genetics and Plant Physiology
Swedish University of Agricultural Sciences, Department of Forest Genetics and Plant Physiology
University of Copenhagen
Gardestrom, Per
Umea University
Guo, Hongwei
Southern University of Science and Technology
UKÄ Subject classification
Botany
Publication Identifiers
DOI: https://doi.org/10.1093/plphys/kiac244
URI (permanent link to this page)
https://res.slu.se/id/publ/117571