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Metabolic control of arginine and ornithine levels paces the progression of leaf senescence
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 sen...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9342962/ https://www.ncbi.nlm.nih.gov/pubmed/35604104 http://dx.doi.org/10.1093/plphys/kiac244 |
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author | Liebsch, Daniela Juvany, Marta Li, Zhonghai Wang, Hou-Ling Ziolkowska, Agnieszka Chrobok, Daria Boussardon, Clément Wen, Xing Law, Simon R Janečková, Helena Brouwer, Bastiaan Lindén, Pernilla Delhomme, Nicolas Stenlund, Hans Moritz, Thomas Gardeström, Per Guo, Hongwei Keech, Olivier |
author_facet | Liebsch, Daniela Juvany, Marta Li, Zhonghai Wang, Hou-Ling Ziolkowska, Agnieszka Chrobok, Daria Boussardon, Clément Wen, Xing Law, Simon R Janečková, Helena Brouwer, Bastiaan Lindén, Pernilla Delhomme, Nicolas Stenlund, Hans Moritz, Thomas Gardeström, Per Guo, Hongwei Keech, Olivier |
author_sort | Liebsch, Daniela |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9342962 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-93429622022-08-02 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, Clément Wen, Xing Law, Simon R Janečková, Helena Brouwer, Bastiaan Lindén, Pernilla Delhomme, Nicolas Stenlund, Hans Moritz, Thomas Gardeström, Per Guo, Hongwei Keech, Olivier Plant Physiol Research Articles 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. Oxford University Press 2022-05-23 /pmc/articles/PMC9342962/ /pubmed/35604104 http://dx.doi.org/10.1093/plphys/kiac244 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Research Articles Liebsch, Daniela Juvany, Marta Li, Zhonghai Wang, Hou-Ling Ziolkowska, Agnieszka Chrobok, Daria Boussardon, Clément Wen, Xing Law, Simon R Janečková, Helena Brouwer, Bastiaan Lindén, Pernilla Delhomme, Nicolas Stenlund, Hans Moritz, Thomas Gardeström, Per Guo, Hongwei Keech, Olivier Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title | Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title_full | Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title_fullStr | Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title_full_unstemmed | Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title_short | Metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
title_sort | metabolic control of arginine and ornithine levels paces the progression of leaf senescence |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9342962/ https://www.ncbi.nlm.nih.gov/pubmed/35604104 http://dx.doi.org/10.1093/plphys/kiac244 |
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