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Review
. 2022 Sep 9:13:961872.
doi: 10.3389/fpls.2022.961872. eCollection 2022.

Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants

Ali Raza  1 , Hajar Salehi  2 , Md Atikur Rahman  3 , Zainab Zahid  4 , Maryam Madadkar Haghjou  5 , Shiva Najafi-Kakavand  6 , Sidra Charagh  7 , Hany S Osman  8 , Mohammed Albaqami  9 , Yuhui Zhuang  10 , Kadambot H M Siddique  11 , Weijian Zhuang  1
Affiliations
Review

Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants

Ali Raza et al. Front Plant Sci. .

Abstract

Due to global climate change, abiotic stresses are affecting plant growth, productivity, and the quality of cultivated crops. Stressful conditions disrupt physiological activities and suppress defensive mechanisms, resulting in stress-sensitive plants. Consequently, plants implement various endogenous strategies, including plant hormone biosynthesis (e.g., abscisic acid, jasmonic acid, salicylic acid, brassinosteroids, indole-3-acetic acid, cytokinins, ethylene, gibberellic acid, and strigolactones) to withstand stress conditions. Combined or single abiotic stress disrupts the normal transportation of solutes, causes electron leakage, and triggers reactive oxygen species (ROS) production, creating oxidative stress in plants. Several enzymatic and non-enzymatic defense systems marshal a plant's antioxidant defenses. While stress responses and the protective role of the antioxidant defense system have been well-documented in recent investigations, the interrelationships among plant hormones, plant neurotransmitters (NTs, such as serotonin, melatonin, dopamine, acetylcholine, and γ-aminobutyric acid), and antioxidant defenses are not well explained. Thus, this review discusses recent advances in plant hormones, transgenic and metabolic developments, and the potential interaction of plant hormones with NTs in plant stress response and tolerance mechanisms. Furthermore, we discuss current challenges and future directions (transgenic breeding and genome editing) for metabolic improvement in plants using modern molecular tools. The interaction of plant hormones and NTs involved in regulating antioxidant defense systems, molecular hormone networks, and abiotic-induced oxidative stress tolerance in plants are also discussed.

Keywords: GABA; abiotic stress; climate change; drought stress; genetic engineering; melatonin; transgenic approach.

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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 role of phytohormones in improving plant tolerance against multiple abiotic stresses. Under stress conditions, phytohormones can modulate the stress intensity in plants by triggering defense mechanisms and thus regulate physio-biochemical processes by increasing plant tolerance to environmental stress. CK, GA, ABA, IAA, and JA mainly play inhibitory roles, whereas BRs, SA, SLs, and ethylene play stimulatory roles in improving several physiological and biochemical mechanisms under stress conditions. Notably, ABA is a primary driving force, playing a vital role alone or combined with other hormones under stress. Furthermore, CKs and auxin play a dual role (inhibitory and stimulatory) by regulating plant growth and development processes.
FIGURE 2
FIGURE 2
Management of ROS metabolism and signaling in plants under stress conditions. Cellular ROS accumulation is controlled by three main methods—(1) ROS generation, (2) ROS scavenging, and (3) ROS transport—which maintain ROS concentrations and produce various ROS signatures and gradients that act as signals in various abiotic factor-response signal transduction pathways. These redox regulations lead to coordinated changes in the plant’s physiology, metabolome, proteome, methylome, and transcriptome. Dashed arrows show that ROS generation, scavenging, and transport can be controlled by the ‘redox state’ of plant cells under stress. Figure based on the concept of Mittler et al. (2004, . For more information on ROS metabolism and signaling, readers are referred to Mittler et al. (2022). ROS, reactive oxygen species; O2, oxygen; H2O, water.
FIGURE 3
FIGURE 3
Oxidative stress in plants and its significance. Under abiotic-stress-induced oxidative stress, ROS generation is the most significant step, which leads to the battle for equilibrium between ROS and antioxidant defense. This involves substantial crosstalk and consequences between stress signals and plant growth and yield reduction. For instance, minor damage caused by oxidative stress can improve growth and yield, whereas extreme oxidative stress can significantly reduce plant growth and yield—modified from Hasanuzzaman et al. (2020a). ROS, reactive oxygen species; H2O2, hydrogen peroxide; O2, oxygen; 1O2, singlet oxygen; 3O2, triplet oxygen; O2∙-, superoxide; OH∙, hydroxyl radical.
FIGURE 4
FIGURE 4
The proposed model demonstrates the state-of-the-art potential of a phytohormone-mediated antioxidant defense system under abiotic stress. Notably, phytohormones decrease the damaging effect of oxidative stress induced by abiotic stress because they act as secondary messengers to initiate antioxidants and can thus scavenge ROS in stressed plants. Interestingly, exogenous phytohormone application can reduce ROS overproduction, enhancing the activities of several antioxidant defense systems and stress tolerance; it varies with the type of stress, plant type, and duration. However, ROS overproduction can significantly reduce growth and yield under stressful conditions. In addition, exogenous phytohormones can increase the production and functionality of endogenous hormones and transcript levels of antioxidant enzyme-encoding genes, e.g., SOD, CAT, and POD. The optimal dose and growth stage for phytohormone application needs further investigation—modified from Raza et al. (2021c) with permission from the publisher (Springer Nature).
FIGURE 5
FIGURE 5
Schematic for improving phytohormone-mediated antioxidant defense via genetic and metabolic engineering using a modern gene-editing tool such as clustered regularly interspaced short palindromic repeats-CRISPR-associated proteins (CRISPR/Cas). Targeted engineering to activate or repress biosynthesis and enzyme-encoding genes can help enhance abiotic-stress-induced oxidative stress in plants by improving the activity of antioxidant defense systems. The genes within the boxes are based on the literature cited in the main text.
FIGURE 6
FIGURE 6
Possible mechanisms for the interaction of neurotransmitters and phytohormones and their roles in several physiological processes. Phytohormones and NTs coordinate as growth regulators, antioxidant activators, redox state managers, and oxidative stress reducers, improving plant growth and enhancing multiple stress tolerances. The illustration presents a series of physiological and biochemical mechanisms linked to the interaction of five NTs with different plant growth regulators. The solid and dashed lines indicate strong and weak interaction, respectively. Lines with bars show the inhibition of a physiological process by NTs. During this process, GABA accumulates rapidly in response to several abiotic stresses. GABA, γ-aminobutyric acid; ABA, abscisic acid; GAs, gibberellic acids; IAA, indole-3-acetic acid; SA, salicylic acid; BRs, brassinosteroids; JS, jasmonic acid; CKs, cytokines; GAs, gibberellic acids; SLs, strigolactones; ET, ethylene; SOD, superoxide dismutase, CAT, catalase; POD, peroxidase; AsA-GSH, ascorbate-glutathione; H2O2, hydrogen peroxide; 1O2, singlet oxygen; O2∙-, superoxide; OH, hydroxyl radical; MDA, malondialdehyde; GB, glycine betaine; Pas, polyamines; UPB1; UPBEAT1 transcription factor; Glu, glutamate; 2-OG, 2-oxoglutarate; TCAs, tricarboxylic acid cycle; SSA, succinic semialdehyde; Succ, succinate.
FIGURE 7
FIGURE 7
Physiological role of neurotransmitters (NTs) associated with plant growth and stress tolerance in plants. NTs coordinate the regulation of plant growth, development, and adaptation/acclimatization, increasing plant stress tolerance. Up/down arrows indicate the increase/decrease of a physiological parameter. GABA, γ-aminobutyric acid; AsA-GSH, ascorbate-glutathione cycle.
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