Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems

Despite the role of γ-aminobutyric acid (GABA) in plant tolerance to chilling stress having been widely discussed in the seedling stage, very little information is clear regarding its implication in chilling tolerance during the reproductive stage of the plant. Here, we investigated the influence of...

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Main Authors: Ola H. Abd Elbar, Amr Elkelish, Gniewko Niedbała, Reham Farag, Tomasz Wojciechowski, Soumya Mukherjee, Ayman F. Abou-Hadid, Hussien M. El-Hennawy, Ahmed Abou El-Yazied, Hany G. Abd El-Gawad, Ehab Azab, Adil A. Gobouri, Nihal El Nahhas, Ahmed M. El-Sawy, Ahmed Bondok, Mohamed F. M. Ibrahim
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.663750/full
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author Ola H. Abd Elbar
Amr Elkelish
Gniewko Niedbała
Reham Farag
Tomasz Wojciechowski
Soumya Mukherjee
Ayman F. Abou-Hadid
Hussien M. El-Hennawy
Ahmed Abou El-Yazied
Hany G. Abd El-Gawad
Ehab Azab
Adil A. Gobouri
Nihal El Nahhas
Ahmed M. El-Sawy
Ahmed Bondok
Mohamed F. M. Ibrahim
author_facet Ola H. Abd Elbar
Amr Elkelish
Gniewko Niedbała
Reham Farag
Tomasz Wojciechowski
Soumya Mukherjee
Ayman F. Abou-Hadid
Hussien M. El-Hennawy
Ahmed Abou El-Yazied
Hany G. Abd El-Gawad
Ehab Azab
Adil A. Gobouri
Nihal El Nahhas
Ahmed M. El-Sawy
Ahmed Bondok
Mohamed F. M. Ibrahim
author_sort Ola H. Abd Elbar
collection DOAJ
description Despite the role of γ-aminobutyric acid (GABA) in plant tolerance to chilling stress having been widely discussed in the seedling stage, very little information is clear regarding its implication in chilling tolerance during the reproductive stage of the plant. Here, we investigated the influence of GABA (1 and 2mM) as a foliar application on tomato plants (Solanum lycopersicum L. cv. Super Marmande) subjected to chilling stress (5°C for 6h/day) for 5 successive days during the flowering stage. The results indicated that applied GABA differentially influenced leaf pigment composition by decreasing the chlorophyll a/b ratio and increasing the anthocyanin relative to total chlorophyll. However, carotenoids were not affected in both GABA-treated and non-treated stressed plants. Root tissues significantly exhibited an increase in thermo-tolerance in GABA-treated plants. Furthermore, applied GABA substantially alleviated the chilling-induced oxidative damage by protecting cell membrane integrity and reducing malondialdehyde (MDA) and H2O2. This positive effect of GABA was associated with enhancing the activity of phenylalanine ammonia-lyase (PAL), catalase (CAT), superoxide dismutase (SOD), and ascorbate peroxidase (APX). Conversely, a downregulation of peroxidase (POX) and polyphenol oxidase (PPO) was observed under chilling stress which indicates its relevance in phenol metabolism. Interesting correlations were obtained between GABA-induced upregulation of sugar metabolism coinciding with altering secondary metabolism, activities of antioxidant enzymes, and maintaining the integrity of plastids’ ultrastructure Eventually, applied GABA especially at 2mM improved the fruit yield and could be recommended to mitigate the damage of chilling stress in tomato plants.
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spelling doaj.art-1e635d787dd849ce9120b3d4630aed502022-12-21T21:23:59ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-10-011210.3389/fpls.2021.663750663750Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense SystemsOla H. Abd Elbar0Amr Elkelish1Gniewko Niedbała2Reham Farag3Tomasz Wojciechowski4Soumya Mukherjee5Ayman F. Abou-Hadid6Hussien M. El-Hennawy7Ahmed Abou El-Yazied8Hany G. Abd El-Gawad9Ehab Azab10Adil A. Gobouri11Nihal El Nahhas12Ahmed M. El-Sawy13Ahmed Bondok14Mohamed F. M. Ibrahim15Department of Agricultural Botany, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Botany, Faculty of Science, Suez Canal University, Ismailia, EgyptDepartment of Biosystems Engineering, Faculty of Environmental and Mechanical Engineering, Poznań University of Life Sciences, Poznań, PolandDepartment of Agricultural Botany, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Biosystems Engineering, Faculty of Environmental and Mechanical Engineering, Poznań University of Life Sciences, Poznań, PolandDepartment of Botany, Jangipur College, University of Kalyani, West Bengal, IndiaDepartment of Horticulture, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Horticulture, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Horticulture, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Horticulture, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Food Science and Nutrition, College of Science, Taif University, Taif, Saudi ArabiaDepartment of Chemistry, College of Science, Taif University, Taif, Saudi ArabiaDepartment of Botany and Microbiology, Faculty of Science, Alexandria University, Alexandria, EgyptDepartment of Climate Modification, Central Laboratory for Agriculture Climate, Agriculture Research Center, Giza, Egypt0Department of Plant Pathology, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDepartment of Agricultural Botany, Faculty of Agriculture, Ain Shams University, Cairo, EgyptDespite the role of γ-aminobutyric acid (GABA) in plant tolerance to chilling stress having been widely discussed in the seedling stage, very little information is clear regarding its implication in chilling tolerance during the reproductive stage of the plant. Here, we investigated the influence of GABA (1 and 2mM) as a foliar application on tomato plants (Solanum lycopersicum L. cv. Super Marmande) subjected to chilling stress (5°C for 6h/day) for 5 successive days during the flowering stage. The results indicated that applied GABA differentially influenced leaf pigment composition by decreasing the chlorophyll a/b ratio and increasing the anthocyanin relative to total chlorophyll. However, carotenoids were not affected in both GABA-treated and non-treated stressed plants. Root tissues significantly exhibited an increase in thermo-tolerance in GABA-treated plants. Furthermore, applied GABA substantially alleviated the chilling-induced oxidative damage by protecting cell membrane integrity and reducing malondialdehyde (MDA) and H2O2. This positive effect of GABA was associated with enhancing the activity of phenylalanine ammonia-lyase (PAL), catalase (CAT), superoxide dismutase (SOD), and ascorbate peroxidase (APX). Conversely, a downregulation of peroxidase (POX) and polyphenol oxidase (PPO) was observed under chilling stress which indicates its relevance in phenol metabolism. Interesting correlations were obtained between GABA-induced upregulation of sugar metabolism coinciding with altering secondary metabolism, activities of antioxidant enzymes, and maintaining the integrity of plastids’ ultrastructure Eventually, applied GABA especially at 2mM improved the fruit yield and could be recommended to mitigate the damage of chilling stress in tomato plants.https://www.frontiersin.org/articles/10.3389/fpls.2021.663750/fulltomato (Solanum lycopersicum L.)gamma-aminobutyric acidchilling stresschloroplast ultrastructureoxidative stressantioxidants
spellingShingle Ola H. Abd Elbar
Amr Elkelish
Gniewko Niedbała
Reham Farag
Tomasz Wojciechowski
Soumya Mukherjee
Ayman F. Abou-Hadid
Hussien M. El-Hennawy
Ahmed Abou El-Yazied
Hany G. Abd El-Gawad
Ehab Azab
Adil A. Gobouri
Nihal El Nahhas
Ahmed M. El-Sawy
Ahmed Bondok
Mohamed F. M. Ibrahim
Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
Frontiers in Plant Science
tomato (Solanum lycopersicum L.)
gamma-aminobutyric acid
chilling stress
chloroplast ultrastructure
oxidative stress
antioxidants
title Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
title_full Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
title_fullStr Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
title_full_unstemmed Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
title_short Protective Effect of γ-Aminobutyric Acid Against Chilling Stress During Reproductive Stage in Tomato Plants Through Modulation of Sugar Metabolism, Chloroplast Integrity, and Antioxidative Defense Systems
title_sort protective effect of γ aminobutyric acid against chilling stress during reproductive stage in tomato plants through modulation of sugar metabolism chloroplast integrity and antioxidative defense systems
topic tomato (Solanum lycopersicum L.)
gamma-aminobutyric acid
chilling stress
chloroplast ultrastructure
oxidative stress
antioxidants
url https://www.frontiersin.org/articles/10.3389/fpls.2021.663750/full
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