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. 2021 Oct 18:12:663750.
doi: 10.3389/fpls.2021.663750. eCollection 2021.

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

Ola H Abd Elbar  1 , Amr Elkelish  2 , Gniewko Niedbała  3 , Reham Farag  1 , Tomasz Wojciechowski  3 , Soumya Mukherjee  4 , Ayman F Abou-Hadid  5 , Hussien M El-Hennawy  5 , Ahmed Abou El-Yazied  5 , Hany G Abd El-Gawad  5 , Ehab Azab  6 , Adil A Gobouri  7 , Ahmed M El-Sawy  8 , Ahmed Bondok  9 , Mohamed F M Ibrahim  1
Affiliations

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

Ola H Abd Elbar et al. Front Plant Sci. .

Erratum in

Abstract

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.

Keywords: antioxidants; chilling stress; chloroplast ultrastructure; fruit yield; gamma-aminobutyric acid; oxidative stress; tomato (Solanum lycopersicum L.).

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
The timeline infographic for the treatments of GABA as a foliar application and the samples’ collection of tomato plants subjected chilling stress in the reproductive stage.
Figure 2
Figure 2
Effect of γ-aminobutyric acid (GABA) as a foliar application at 1 and 2mM on leaf pigments concentration of tomato plants cv “Super marmende” growing under normal (25°C/20°C day/night ) and chilling conditions (5 days/4ºC for 6 h/day) followed by 2 days recovery. (A), chlorophyll a; (B), chlorophyll b; (C), total chlorophyll; (D), chlorophyll a/b ratio; (E), carotenoids, and (F), anthocyanin. Data followed by the same letters ± SE are not significant according to Duncan multiple rang test at P≤0.05. The white columns refer to the control conditions and the black columns refer to the chilling stress.
Figure 3
Figure 3
Effect of γ-aminobutyric acid (GABA) as a foliar application at 1 and 2mM on carbohydrate concentration of tomato plants cv “Super marmende” growing under normal (25°C/20°C day/night ) and chilling conditions (5 days/4ºC for 6h/day) followed by 2 days recovery. (A), reducing sugars; (B), non-reducing sugars and (C), total soluble sugars. Data followed by the same letters ± SE are not significant according to Duncan multiple rang test at P≤0.05. The white columns refer to the control conditions and the black columns refer to the chilling stress.
Figure 4
Figure 4
Effect of γ-aminobutyric acid (GABA) as a foliar application at 1 and 2mM on leaf oxidative damage and root tissues thermotolerance of tomato plants cv “Super marmende” growing under normal (25°C/20°C day/night ) and chilling conditions (5 days/4ºC for 6h/day) followed by 2 days recovery. (A), hydrogen peroxide (H2O2); (B), malondialdehyde (MDA); (C), electrolyte leakage, and (D), root thermotolerance as reduced TTC. Data followed by the same letters ± SE are not significant according to Duncan multiple rang test P≤0.05. The white columns refer to the control conditions and the black columns refer to the chilling stress.
Figure 5
Figure 5
Effect of γ-aminobutyric acid (GABA) as a foliar application at 1 and 2mM on antioxidant and phenolic-related enzymes of tomato plants cv “Super marmende” growing under normal (25°C/20°C day/night ) and chilling conditions (5 days/4ºC for 6 h/day) followed by 2 days recovery. (A), superoxide dismutase (SOD); (B), catalase (CAT); (C), polyphenol oxidase (PPO); (D), peroxidase (POD); (E), ascorbate peroxidase (APX), and (F), phenylalanine ammonia lyase (PAL). Data followed by the same letters ± SE are not significant according to Duncan multiple rang test at P≤0.05. The white columns refer to the control conditions and the black columns refer to the chilling stress.
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