TY - JOUR

T1 - Metabolic control of arginine and ornithine levels paces the progression of leaf senescence

AU - Liebsch, Daniela

AU - Juvany, Marta

AU - Li, Zhonghai

AU - Wang, Hou-Ling

AU - Ziolkowska, Agnieszka

AU - Chrobok, Daria

AU - Boussardon, Clément

AU - Wen, Xing

AU - Law, Simon R

AU - Janečková, Helena

AU - Brouwer, Bastiaan

AU - Lindén, Pernilla

AU - Delhomme, Nicolas

AU - Stenlund, Hans

AU - Moritz, Thomas

AU - Gardeström, Per

AU - Guo, Hongwei

AU - Keech, Olivier

N1 - © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists.

PY - 2022

Y1 - 2022

N2 - 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, i.e., 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 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 is controlled in an age-dependent manner. Thirdly, we demonstrate that spermidine 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 amino acid 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.

AB - 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, i.e., 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 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 is controlled in an age-dependent manner. Thirdly, we demonstrate that spermidine 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 amino acid 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.

U2 - 10.1093/plphys/kiac244

DO - 10.1093/plphys/kiac244

M3 - Journal article

C2 - 35604104

VL - 189

SP - 1943

EP - 1960

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 4

ER -