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Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress

Aluminum (Al) toxicity is a major threat to global crop production in acidic soils, which can be mitigated by natural substances such as pyroligneous acid (PA). However, the effect of PA in regulating plant central carbon metabolism (CCM) under Al stress is unknown. In this study, we investigated th...

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Autores principales: Ofoe, Raphael, Thomas, Raymond H., Abbey, Lord
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10303050/
https://www.ncbi.nlm.nih.gov/pubmed/37367927
http://dx.doi.org/10.3390/metabo13060770
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author Ofoe, Raphael
Thomas, Raymond H.
Abbey, Lord
author_facet Ofoe, Raphael
Thomas, Raymond H.
Abbey, Lord
author_sort Ofoe, Raphael
collection PubMed
description Aluminum (Al) toxicity is a major threat to global crop production in acidic soils, which can be mitigated by natural substances such as pyroligneous acid (PA). However, the effect of PA in regulating plant central carbon metabolism (CCM) under Al stress is unknown. In this study, we investigated the effects of varying PA concentrations (0, 0.25 and 1% PA/ddH(2)O (v/v)) on intermediate metabolites involved in CCM in tomato (Solanum lycopersicum L., ‘Scotia’) seedlings under varying Al concentrations (0, 1 and 4 mM AlCl(3)). A total of 48 differentially expressed metabolites of CCM were identified in the leaves of both control and PA-treated plants under Al stress. Calvin–Benson cycle (CBC) and pentose phosphate pathway (PPP) metabolites were considerably reduced under 4 mM Al stress, irrespective of the PA treatment. Conversely, the PA treatment markedly increased glycolysis and tricarboxylic acid cycle (TCA) metabolites compared to the control. Although glycolysis metabolites in the 0.25% PA-treated plants under Al stress were comparable to the control, the 1% PA-treated plants exhibited the highest accumulation of glycolysis metabolites. Furthermore, all PA treatments increased TCA metabolites under Al stress. Electron transport chain (ETC) metabolites were higher in PA-treated plants alone and under 1 mM, Al but were reduced under a higher Al treatment of 4 mM. Pearson correlation analysis revealed that CBC metabolites had a significantly strong positive (r = 0.99; p < 0.001) association with PPP metabolites. Additionally, glycolysis metabolites showed a significantly moderate positive association (r = 0.76; p < 0.05) with TCA metabolites, while ETC metabolites exhibited no association with any of the determined pathways. The coordinated association between CCM pathway metabolites suggests that PA can stimulate changes in plant metabolism to modulate energy production and biosynthesis of organic acids under Al stress conditions.
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spelling pubmed-103030502023-06-29 Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress Ofoe, Raphael Thomas, Raymond H. Abbey, Lord Metabolites Article Aluminum (Al) toxicity is a major threat to global crop production in acidic soils, which can be mitigated by natural substances such as pyroligneous acid (PA). However, the effect of PA in regulating plant central carbon metabolism (CCM) under Al stress is unknown. In this study, we investigated the effects of varying PA concentrations (0, 0.25 and 1% PA/ddH(2)O (v/v)) on intermediate metabolites involved in CCM in tomato (Solanum lycopersicum L., ‘Scotia’) seedlings under varying Al concentrations (0, 1 and 4 mM AlCl(3)). A total of 48 differentially expressed metabolites of CCM were identified in the leaves of both control and PA-treated plants under Al stress. Calvin–Benson cycle (CBC) and pentose phosphate pathway (PPP) metabolites were considerably reduced under 4 mM Al stress, irrespective of the PA treatment. Conversely, the PA treatment markedly increased glycolysis and tricarboxylic acid cycle (TCA) metabolites compared to the control. Although glycolysis metabolites in the 0.25% PA-treated plants under Al stress were comparable to the control, the 1% PA-treated plants exhibited the highest accumulation of glycolysis metabolites. Furthermore, all PA treatments increased TCA metabolites under Al stress. Electron transport chain (ETC) metabolites were higher in PA-treated plants alone and under 1 mM, Al but were reduced under a higher Al treatment of 4 mM. Pearson correlation analysis revealed that CBC metabolites had a significantly strong positive (r = 0.99; p < 0.001) association with PPP metabolites. Additionally, glycolysis metabolites showed a significantly moderate positive association (r = 0.76; p < 0.05) with TCA metabolites, while ETC metabolites exhibited no association with any of the determined pathways. The coordinated association between CCM pathway metabolites suggests that PA can stimulate changes in plant metabolism to modulate energy production and biosynthesis of organic acids under Al stress conditions. MDPI 2023-06-20 /pmc/articles/PMC10303050/ /pubmed/37367927 http://dx.doi.org/10.3390/metabo13060770 Text en © 2023 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
Ofoe, Raphael
Thomas, Raymond H.
Abbey, Lord
Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title_full Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title_fullStr Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title_full_unstemmed Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title_short Coordinated Regulation of Central Carbon Metabolism in Pyroligneous Acid-Treated Tomato Plants under Aluminum Stress
title_sort coordinated regulation of central carbon metabolism in pyroligneous acid-treated tomato plants under aluminum stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10303050/
https://www.ncbi.nlm.nih.gov/pubmed/37367927
http://dx.doi.org/10.3390/metabo13060770
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