Alterations of Endogenous Hormones, Antioxidant Metabolism, and Aquaporin Gene Expression in Relation to γ-Aminobutyric Acid-Regulated Thermotolerance in White Clover

Abstract

Persistent high temperature decreases the yield and quality of crops, including many important herbs. White clover (Trifolium repens) is a perennial herb with high feeding and medicinal value, but is sensitive to temperatures above 30 °C. The present study was conducted to elucidate the impact of changes in endogenous γ-aminobutyric acid (GABA) level by exogenous GABA pretreatment on heat tolerance of white clover, associated with alterations in endogenous hormones, antioxidant metabolism, and aquaporin-related gene expression in root and leaf of white clover plants under high-temperature stress. Our results reveal that improvement in endogenous GABA level in leaf and root by GABA pretreatment could significantly alleviate the damage to white clover during high-temperature stress, as demonstrated by enhancements in cell membrane stability, photosynthetic capacity, and osmotic adjustment ability, as well as lower oxidative damage and chlorophyll loss. The GABA significantly enhanced gene expression and enzyme activities involved in antioxidant defense, including superoxide dismutase, catalase, peroxidase, and key enzymes of the ascorbic acid–glutathione cycle, thus reducing the accumulation of reactive oxygen species and the oxidative injury to membrane lipids and proteins. The GABA also increased endogenous indole-3-acetic acid content in roots and leaves and cytokinin content in leaves, associated with growth maintenance and reduced leaf senescence under heat stress. The GABA significantly upregulated the expression of PIP1-1 and PIP2-7 in leaves and the TIP2-1 expression in leaves and roots under high temperature, and also alleviated the heat-induced inhibition of PIP1-1, PIP2-2, TIP2-2, and NIP1-2 expression in roots, which could help to improve the water transportation and homeostasis from roots to leaves. In addition, the GABA-induced aquaporins expression and decline in endogenous abscisic acid level could improve the heat dissipation capacity through maintaining higher stomatal opening and transpiration in white clovers under high-temperature stress.

The role of γ-aminobutyric acid and salicylic acid in heat stress tolerance under salinity conditions in Origanum vulgare L.

“…GABA pretreatment could induce endogenous GABA levels and subsequently improve physiological effects associated with high temperature in Trifolium repens plants. Pretreatment with GABA considerably regulated osmotic adjustment, enhanced photosynthetic, improve cell membrane stability, reduced oxidative damage and increased plant tolerance to HT stress [48]. GABA treatment had healing effects such as improving germination rate, seedling length, fresh and dry weights of the shoot, carbon and nitrogen concentrations in 175 mM NaCl-treated Lolium perenne L. [49].…”

A Trifolium repens flavodoxin‐like quinone reductase 1 (TrFQR1) improves plant adaptability to high temperature associated with oxidative homeostasis and lipids remodeling

“…Oxidative damage was one of the most deleterious consequences induced by the overaccumulation of ROS in white clover and other cool‐season plants under high‐temperature stress (Liu et al., 2021; Luo et al., 2020; Yu et al., 2022). In response to heat stress, significant enhancement of ROS‐scavenging enzyme activities such as SOD and multiple other enzymes involved in the ASA‐GSH cycle has been found to be associated with alleviation of oxidative damage in plants (Buttar et al., 2020; Li et al., 2016; Qi et al., 2021). However, a substantial previous study only focused on investigating the critical role of enhanced ROS‐scavenging systems in mitigating oxidative damage under abiotic stress, but neglected the importance of manipulative ROS origin to redox equilibrium and ROS homeostasis when plants underwent unfavorable environment conditions.…”

Metabolic Regulation and Lipidomic Remodeling in Relation to Spermidine-induced Stress Tolerance to High Temperature in Plants

“…Oxidative burst and overaccumulation of oxidizing agents damage the cell membrane system, which is one of the major stress symptoms in plants subjected to a prolonged period of heat stress and other abiotic stresses [ 15 , 16 , 17 , 18 ]. Therefore, the maintenance of the structural integrity of the membrane is beneficial to the stress defense system [ 19 ].…”