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Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass

Soil salinization has become a serious challenge to modern agriculture worldwide. The purpose of the study was to reveal salt tolerance induced by spermine (Spm) associated with alterations in water and redox homeostasis, photosynthetic performance, and global metabolites reprogramming based on anal...

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Autores principales: Li, Zhou, Cheng, Bizhen, Liu, Wei, Feng, Guangyan, Zhao, Junming, Zhang, Liquan, Peng, Yan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9104555/
https://www.ncbi.nlm.nih.gov/pubmed/35562863
http://dx.doi.org/10.3390/ijms23094472
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author Li, Zhou
Cheng, Bizhen
Liu, Wei
Feng, Guangyan
Zhao, Junming
Zhang, Liquan
Peng, Yan
author_facet Li, Zhou
Cheng, Bizhen
Liu, Wei
Feng, Guangyan
Zhao, Junming
Zhang, Liquan
Peng, Yan
author_sort Li, Zhou
collection PubMed
description Soil salinization has become a serious challenge to modern agriculture worldwide. The purpose of the study was to reveal salt tolerance induced by spermine (Spm) associated with alterations in water and redox homeostasis, photosynthetic performance, and global metabolites reprogramming based on analyses of physiological responses and metabolomics in creeping bentgrass (Agrostis stolonifera). Plants pretreated with or without 0.5 mM Spm were subjected to salt stress induced by NaCl for 25 days in controlled growth chambers. Results showed that a prolonged period of salt stress caused a great deal of sodium (Na) accumulation, water loss, photoinhibition, and oxidative damage to plants. However, exogenous application of Spm significantly improved endogenous spermidine (Spd) and Spm contents, followed by significant enhancement of osmotic adjustment (OA), photosynthesis, and antioxidant capacity in leaves under salt stress. The Spm inhibited salt-induced Na accumulation but did not affect potassium (K) content. The analysis of metabolomics demonstrated that the Spm increased intermediate metabolites of γ-aminobutyric acid (GABA) shunt (GABA, glutamic acid, and alanine) and tricarboxylic acid (TCA) cycle (aconitic acid) under salt stress. In addition, the Spm also up-regulated the accumulation of multiple amino acids (glutamine, valine, isoleucine, methionine, serine, lysine, tyrosine, phenylalanine, and tryptophan), sugars (mannose, fructose, sucrose-6-phosphate, tagatose, and cellobiose), organic acid (gallic acid), and other metabolites (glycerol) in response to salt stress. These metabolites played important roles in OA, energy metabolism, signal transduction, and antioxidant defense under salt stress. More importantly, the Spm enhanced GABA shunt and the TCA cycle for energy supply in leaves. Current findings provide new evidence about the regulatory roles of the Spm in alleviating salt damage to plants associated with global metabolites reprogramming and metabolic homeostasis.
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spelling pubmed-91045552022-05-14 Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass Li, Zhou Cheng, Bizhen Liu, Wei Feng, Guangyan Zhao, Junming Zhang, Liquan Peng, Yan Int J Mol Sci Article Soil salinization has become a serious challenge to modern agriculture worldwide. The purpose of the study was to reveal salt tolerance induced by spermine (Spm) associated with alterations in water and redox homeostasis, photosynthetic performance, and global metabolites reprogramming based on analyses of physiological responses and metabolomics in creeping bentgrass (Agrostis stolonifera). Plants pretreated with or without 0.5 mM Spm were subjected to salt stress induced by NaCl for 25 days in controlled growth chambers. Results showed that a prolonged period of salt stress caused a great deal of sodium (Na) accumulation, water loss, photoinhibition, and oxidative damage to plants. However, exogenous application of Spm significantly improved endogenous spermidine (Spd) and Spm contents, followed by significant enhancement of osmotic adjustment (OA), photosynthesis, and antioxidant capacity in leaves under salt stress. The Spm inhibited salt-induced Na accumulation but did not affect potassium (K) content. The analysis of metabolomics demonstrated that the Spm increased intermediate metabolites of γ-aminobutyric acid (GABA) shunt (GABA, glutamic acid, and alanine) and tricarboxylic acid (TCA) cycle (aconitic acid) under salt stress. In addition, the Spm also up-regulated the accumulation of multiple amino acids (glutamine, valine, isoleucine, methionine, serine, lysine, tyrosine, phenylalanine, and tryptophan), sugars (mannose, fructose, sucrose-6-phosphate, tagatose, and cellobiose), organic acid (gallic acid), and other metabolites (glycerol) in response to salt stress. These metabolites played important roles in OA, energy metabolism, signal transduction, and antioxidant defense under salt stress. More importantly, the Spm enhanced GABA shunt and the TCA cycle for energy supply in leaves. Current findings provide new evidence about the regulatory roles of the Spm in alleviating salt damage to plants associated with global metabolites reprogramming and metabolic homeostasis. MDPI 2022-04-19 /pmc/articles/PMC9104555/ /pubmed/35562863 http://dx.doi.org/10.3390/ijms23094472 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Li, Zhou
Cheng, Bizhen
Liu, Wei
Feng, Guangyan
Zhao, Junming
Zhang, Liquan
Peng, Yan
Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title_full Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title_fullStr Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title_full_unstemmed Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title_short Global Metabolites Reprogramming Induced by Spermine Contributing to Salt Tolerance in Creeping Bentgrass
title_sort global metabolites reprogramming induced by spermine contributing to salt tolerance in creeping bentgrass
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9104555/
https://www.ncbi.nlm.nih.gov/pubmed/35562863
http://dx.doi.org/10.3390/ijms23094472
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