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Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves

Quercus mongolica is a common landscape, afforestation, and construction timber species in northern China with high ecological, economic, and ornamental value. Leaf senescence is a complex process that has important implications for plant growth and development. To explore changes of metabolites dur...

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Autores principales: Yuan, Yangchen, Zhang, Weiqiang, Pang, Jiushuai, Zhou, Miaomiao, Liu, Jianying, Zhao, Jin, Sui, Jinming, Huang, Dazhuang, Yang, Minsheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10446833/
https://www.ncbi.nlm.nih.gov/pubmed/37611226
http://dx.doi.org/10.1371/journal.pone.0289272
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author Yuan, Yangchen
Zhang, Weiqiang
Pang, Jiushuai
Zhou, Miaomiao
Liu, Jianying
Zhao, Jin
Sui, Jinming
Huang, Dazhuang
Yang, Minsheng
author_facet Yuan, Yangchen
Zhang, Weiqiang
Pang, Jiushuai
Zhou, Miaomiao
Liu, Jianying
Zhao, Jin
Sui, Jinming
Huang, Dazhuang
Yang, Minsheng
author_sort Yuan, Yangchen
collection PubMed
description Quercus mongolica is a common landscape, afforestation, and construction timber species in northern China with high ecological, economic, and ornamental value. Leaf senescence is a complex process that has important implications for plant growth and development. To explore changes of metabolites during the ageing of Quercus mongolica leaves, we investigated physiological responses and metabolite composition in ageing leaves harvested from 15–20-year-old Quercus mongolica. Leaf samples of Q. mongolica were collected when they were still green (at maturity) (stage 1), during early senescence (stage 2), and during late senescence (stage 3). These leaves were then subjected to physiological index and metabolome sequencing analyses. The physiological analysis showed that the leaves of Q. mongolica changed from green to yellow during senescence, which induced significant accumulation of soluble sugar and significant reductions in the concentration of soluble protein and chlorophyll. Peroxidase and catalase were the main antioxidant enzymes mitigating leaf senescence. Metabolomic analysis identified 797 metabolites during leaf senescence. Compared to stage 1, 70 differential metabolites were screened in stage 2 and 72 were screened in stage 3. Differential metabolites in the two senescent stages were principally enriched in amino acid metabolism, lipid metabolism and secondary metabolite biosynthesis. The contents of N-oleoylethanolamine and N, N-dimethylglycine were significantly increased only in stage 2, while the contents of trifolin, astragalin, valine, isoleucine, leucine, and citric acid were significantly increased only in stage 3. Histidine, homoserine, tryptophan, tyrosine, phenylalanine, proline, norleucine, N-glycyl-L-leucine, linoleic acid, linolenic acid, gallic acid, 3-indoleacrylic acid, 3-amino-2-naphthoic acid, 3-hydroxy-3-methylpentane-1,5-dioic acid, 2,3,4-trihydroxybenzoic acid, trifolin, astragalin, DL-2-aminoadipic acid, pinoresinol dimethyl ether, dimethylmatairesinol, and lysophosphatidylcholine increased during both stage 2 and stage 3. Increasing contents of these metabolites may constitute the main mechanism by which Q. mongolica leaves adapt to senescence.
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spelling pubmed-104468332023-08-24 Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves Yuan, Yangchen Zhang, Weiqiang Pang, Jiushuai Zhou, Miaomiao Liu, Jianying Zhao, Jin Sui, Jinming Huang, Dazhuang Yang, Minsheng PLoS One Research Article Quercus mongolica is a common landscape, afforestation, and construction timber species in northern China with high ecological, economic, and ornamental value. Leaf senescence is a complex process that has important implications for plant growth and development. To explore changes of metabolites during the ageing of Quercus mongolica leaves, we investigated physiological responses and metabolite composition in ageing leaves harvested from 15–20-year-old Quercus mongolica. Leaf samples of Q. mongolica were collected when they were still green (at maturity) (stage 1), during early senescence (stage 2), and during late senescence (stage 3). These leaves were then subjected to physiological index and metabolome sequencing analyses. The physiological analysis showed that the leaves of Q. mongolica changed from green to yellow during senescence, which induced significant accumulation of soluble sugar and significant reductions in the concentration of soluble protein and chlorophyll. Peroxidase and catalase were the main antioxidant enzymes mitigating leaf senescence. Metabolomic analysis identified 797 metabolites during leaf senescence. Compared to stage 1, 70 differential metabolites were screened in stage 2 and 72 were screened in stage 3. Differential metabolites in the two senescent stages were principally enriched in amino acid metabolism, lipid metabolism and secondary metabolite biosynthesis. The contents of N-oleoylethanolamine and N, N-dimethylglycine were significantly increased only in stage 2, while the contents of trifolin, astragalin, valine, isoleucine, leucine, and citric acid were significantly increased only in stage 3. Histidine, homoserine, tryptophan, tyrosine, phenylalanine, proline, norleucine, N-glycyl-L-leucine, linoleic acid, linolenic acid, gallic acid, 3-indoleacrylic acid, 3-amino-2-naphthoic acid, 3-hydroxy-3-methylpentane-1,5-dioic acid, 2,3,4-trihydroxybenzoic acid, trifolin, astragalin, DL-2-aminoadipic acid, pinoresinol dimethyl ether, dimethylmatairesinol, and lysophosphatidylcholine increased during both stage 2 and stage 3. Increasing contents of these metabolites may constitute the main mechanism by which Q. mongolica leaves adapt to senescence. Public Library of Science 2023-08-23 /pmc/articles/PMC10446833/ /pubmed/37611226 http://dx.doi.org/10.1371/journal.pone.0289272 Text en © 2023 Yuan et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yuan, Yangchen
Zhang, Weiqiang
Pang, Jiushuai
Zhou, Miaomiao
Liu, Jianying
Zhao, Jin
Sui, Jinming
Huang, Dazhuang
Yang, Minsheng
Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title_full Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title_fullStr Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title_full_unstemmed Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title_short Integrated physiological and metabolomic analyses reveal changes during the natural senescence of Quercus mongolica leaves
title_sort integrated physiological and metabolomic analyses reveal changes during the natural senescence of quercus mongolica leaves
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10446833/
https://www.ncbi.nlm.nih.gov/pubmed/37611226
http://dx.doi.org/10.1371/journal.pone.0289272
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