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

Hongyin Qi,Yan Zhang,Muhammad Jawad Hassan,Guangyan Feng,Dingfan Kang,Xinquan Zhang,Zhou Li,Yan Peng,Weihang Zeng

doi:10.3390/antiox10071099

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.

Highlights

The objective of the present study was to determine the impact of GABA on improvement in thermotolerance associated with alterations of endogenous hormones, antioxidant metabolism, water regulation, and AQP-related gene transcript level in leaf and root of white clover
The GABA-regulated genes encoding antioxidant enzymes were consistent with the enzyme activities under heat stress. These findings indicate that GABA helped to maintain antioxidant metabolism in leaves and roots of white clover through regulating enzyme activities and gene expression under heat stress
Our results demonstrate that white clover plants pretreated with GABA exhibited significantly higher stomatal conductance and transpiration rate, which could be contributed to better thermolysis of white clover under heat stress

Summary

Introduction

The major impact of global warming is already discernible in animal and plant populations [1]. A global high temperature has resulted in the increase in mortality of forest trees [2], substantial reduction in crop yield [3], and changes in the spatial distribution of herbs [4]. Plant hormones and other plant growth regulators (PGRs) perform pivotal functions in regulating plant adaptability to different abiotic stresses. Γ-aminobutyric acid (GABA), a non-protein amino acid comprising four carbons, exists abundantly in living organisms including microbes, plants, and vertebrates. Over the past 50 years, GABA has been regarded as a very important PGR that affects plant growth

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