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

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  • Daniela Liebsch
  • Marta Juvany
  • Zhonghai Li
  • Hou-Ling Wang
  • Agnieszka Ziolkowska
  • Daria Chrobok
  • Clément Boussardon
  • Xing Wen
  • Simon R Law
  • Helena Janečková
  • Bastiaan Brouwer
  • Pernilla Lindén
  • Nicolas Delhomme
  • Hans Stenlund
  • Moritz, Thomas
  • Per Gardeström
  • Hongwei Guo
  • Olivier Keech

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.

Original languageEnglish
JournalPlant Physiology
Issue number4
Pages (from-to)1943-1960
Publication statusPublished - 2022

Bibliographical note

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

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