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Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants

Trehalose (Tre), which was an osmoprotective or stabilizing molecule, played a protective role against different abiotic stresses in plants and showed remarkable perspectives in salt stress. In this study, the potential role of Tre in improving the resistance to salt stress in tomato plants was inve...

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Autores principales: Yang, Yan, Xie, Jianming, Li, Jing, Zhang, Jing, Zhang, Xiaodan, Yao, Yandong, Wang, Cheng, Niu, Tianhang, Bakpa, Emily Patience
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9412767/
https://www.ncbi.nlm.nih.gov/pubmed/36035709
http://dx.doi.org/10.3389/fpls.2022.974507
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author Yang, Yan
Xie, Jianming
Li, Jing
Zhang, Jing
Zhang, Xiaodan
Yao, Yandong
Wang, Cheng
Niu, Tianhang
Bakpa, Emily Patience
author_facet Yang, Yan
Xie, Jianming
Li, Jing
Zhang, Jing
Zhang, Xiaodan
Yao, Yandong
Wang, Cheng
Niu, Tianhang
Bakpa, Emily Patience
author_sort Yang, Yan
collection PubMed
description Trehalose (Tre), which was an osmoprotective or stabilizing molecule, played a protective role against different abiotic stresses in plants and showed remarkable perspectives in salt stress. In this study, the potential role of Tre in improving the resistance to salt stress in tomato plants was investigated. Tomato plants (Micro Tom) were treated with Hoagland nutrient solution (CK), 10 mM Tre (T), 150 mM sodium chloride (NaCl, S), and 10 mM Tre+150 mM NaCl (S+T) for 5 days. Our results showed that foliar application of Tre alleviated the inhibition of tomato plant growth under salt stress. In addition, salt stress decreased the values of net photosynthetic rate (Pn, 85.99%), stomata conductance (gs, 57.3%), and transpiration rate (Tr, 47.97%), but increased that of intercellular carbon dioxide concentration (Ci, 26.25%). However, exogenous application of Tre significantly increased photosynthetic efficiency, increased the activity of Calvin cycle enzymes [ribulose diphosphate carboxylase/oxygenase (Rubisco), fructose-1,6-bisphosphate aldolase (FBA), fructose-1, 6-bisphosphatase (FBPase), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and transketolase (TK)], up-regulated the expression of genes encoding enzymes, induced stomatal opening, and alleviated salt-induced damage to the chloroplast membrane and structure. In the saline environment, photosynthetic electron transport was restricted, resulting the J-I-P phase to decrease. At the same time, the absorption, capture, and transport energies per excited cross-section and per active reaction center decreased, and the dissipation energy increased. Conversely, Tre reversed these values and enhanced the photosystem response to salt stress by protecting the photosynthetic electron transport system. In addition, foliage application with Tre significantly increased the potassium to sodium transport selectivity ratio (S(K–Na)) by 16.08%, and increased the levels of other ions to varying degrees. Principal component analysis (PCA) analysis showed that exogenous Tre could change the distribution of elements in different organs and affect the expressions of SlSOS1, SlNHX, SlHKT1.1, SlVHA, and SlHA-A at the transcriptional level under salt stress, thereby maintaining ion homeostasis. This study demonstrated that Tre was involved in the process of mitigating salt stress toxicity in tomato plants and provided specific insights into the effectiveness of Tre in mediating salt tolerance.
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spelling pubmed-94127672022-08-27 Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants Yang, Yan Xie, Jianming Li, Jing Zhang, Jing Zhang, Xiaodan Yao, Yandong Wang, Cheng Niu, Tianhang Bakpa, Emily Patience Front Plant Sci Plant Science Trehalose (Tre), which was an osmoprotective or stabilizing molecule, played a protective role against different abiotic stresses in plants and showed remarkable perspectives in salt stress. In this study, the potential role of Tre in improving the resistance to salt stress in tomato plants was investigated. Tomato plants (Micro Tom) were treated with Hoagland nutrient solution (CK), 10 mM Tre (T), 150 mM sodium chloride (NaCl, S), and 10 mM Tre+150 mM NaCl (S+T) for 5 days. Our results showed that foliar application of Tre alleviated the inhibition of tomato plant growth under salt stress. In addition, salt stress decreased the values of net photosynthetic rate (Pn, 85.99%), stomata conductance (gs, 57.3%), and transpiration rate (Tr, 47.97%), but increased that of intercellular carbon dioxide concentration (Ci, 26.25%). However, exogenous application of Tre significantly increased photosynthetic efficiency, increased the activity of Calvin cycle enzymes [ribulose diphosphate carboxylase/oxygenase (Rubisco), fructose-1,6-bisphosphate aldolase (FBA), fructose-1, 6-bisphosphatase (FBPase), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and transketolase (TK)], up-regulated the expression of genes encoding enzymes, induced stomatal opening, and alleviated salt-induced damage to the chloroplast membrane and structure. In the saline environment, photosynthetic electron transport was restricted, resulting the J-I-P phase to decrease. At the same time, the absorption, capture, and transport energies per excited cross-section and per active reaction center decreased, and the dissipation energy increased. Conversely, Tre reversed these values and enhanced the photosystem response to salt stress by protecting the photosynthetic electron transport system. In addition, foliage application with Tre significantly increased the potassium to sodium transport selectivity ratio (S(K–Na)) by 16.08%, and increased the levels of other ions to varying degrees. Principal component analysis (PCA) analysis showed that exogenous Tre could change the distribution of elements in different organs and affect the expressions of SlSOS1, SlNHX, SlHKT1.1, SlVHA, and SlHA-A at the transcriptional level under salt stress, thereby maintaining ion homeostasis. This study demonstrated that Tre was involved in the process of mitigating salt stress toxicity in tomato plants and provided specific insights into the effectiveness of Tre in mediating salt tolerance. Frontiers Media S.A. 2022-08-12 /pmc/articles/PMC9412767/ /pubmed/36035709 http://dx.doi.org/10.3389/fpls.2022.974507 Text en Copyright © 2022 Yang, Xie, Li, Zhang, Zhang, Yao, Wang, Niu and Bakpa. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Yang, Yan
Xie, Jianming
Li, Jing
Zhang, Jing
Zhang, Xiaodan
Yao, Yandong
Wang, Cheng
Niu, Tianhang
Bakpa, Emily Patience
Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title_full Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title_fullStr Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title_full_unstemmed Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title_short Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
title_sort trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9412767/
https://www.ncbi.nlm.nih.gov/pubmed/36035709
http://dx.doi.org/10.3389/fpls.2022.974507
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