Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions

Abstract

Plant glutathione S-transferases (GSTs) are ubiquitous and multifunctional enzymes encoded by large gene families. A characteristic feature of GST genes is their high inducibility by a wide range of stress conditions including biotic stress. Early studies on the role of GSTs in plant biotic stress showed that certain GST genes are specifically up-regulated by microbial infections. Later numerous transcriptome-wide investigations proved that distinct groups of GSTs are markedly induced in the early phase of bacterial, fungal and viral infections. Proteomic investigations also confirmed the accumulation of multiple GST proteins in infected plants. Furthermore, functional studies revealed that overexpression or silencing of specific GSTs can markedly modify disease symptoms and also pathogen multiplication rates. However, very limited information is available about the exact metabolic functions of disease-induced GST isoenzymes and about their endogenous substrates. The already recognized roles of GSTs are the detoxification of toxic substances by their conjugation with glutathione, the attenuation of oxidative stress and the participation in hormone transport. Some GSTs display glutathione peroxidase activity and these GSTs can detoxify toxic lipid hydroperoxides that accumulate during infections. GSTs can also possess ligandin functions and participate in the intracellular transport of auxins. Notably, the expression of multiple GSTs is massively activated by salicylic acid and some GST enzymes were demonstrated to be receptor proteins of salicylic acid. Furthermore, induction of GST genes or elevated GST activities have often been observed in plants treated with beneficial microbes (bacteria and fungi) that induce a systemic resistance response (ISR) to subsequent pathogen infections. Further research is needed to reveal the exact metabolic functions of GST isoenzymes in infected plants and to understand their contribution to disease resistance.

Keywords: WRKY; bacterium; fungus; glutathione S-transferase; oxidative stress; plant pathogen; salicylic acid; virus.

Figure 1

Typical chemical reactions catalyzed by plant glutathione S-transferase (GST) enzymes. (A) Nucleophilic substitution reaction between 1-chloro-2,4-dinitrobenzene (CDNB) and reduced glutathione (GSH). CDNB has been extensively used as a xenobiotic model substrate for GST activity determination (Habig et al., 1974). (B) Nucleophilic addition reaction between cinnamic acid and GSH (Edwards and Dixon, 1991). (C) Reduction (detoxification) of fatty acid hydroperoxides to corresponding hydroxy derivatives by the peroxidase activity of GST as described by Bartling et al. (1993). The substrate 13(S)-hydroperoxy-9,11,15-octadecatrienoic acid was found to accumulate during membrane-damaging lipid peroxidation in infected plants (Wagner et al., 2002).

Figure 2

Dendrograms of the most significantly activated Arabidopsis thaliana glutathione S-transferase (GST) genes following a fungal or a bacterial infection. Below the abbreviated gene names the magnitudes of gene inductions are shown (X =-fold). (A) More than 5-fold up-regulated GSTs at 48 h following infection of A. thaliana with the necrotrophic fungal pathogen Alternaria brassicicola. (B) More than 10-fold up-regulated GSTs at 12 h following infection of A. thaliana with the Pseudomonas syringae pv. tomato DC3000 strain carrying the avrRpt2 effector gene (incompatible interaction). The expression data obtained by De Vos et al. (2005) were collected from the NCBI Gene Expression Omnibus database.

Figure 3

Schematic representation of the disease-related W-box and WT-box cis-regulatory elements in the promoter sequences of eight Arabidopsis thaliana glutathione S-transferase (GST) genes. These sequence motifs are the binding sites of WRKY transcription factor proteins. For in silico analyses 1,500 bp DNA segments upstream of the transcription start sites (TSS) were selected from the NCBI GenBank database. In the case of the GSTF8 gene the promoter of the shorter transcript variant (GSTF8_S) (Thatcher et al., 2007) was analyzed. Symbols: red triangles, W-boxes; blue triangles, WT-boxes. Promoter motifs were found on both DNA strands, which is represented by the orientation of the red and blue symbols. The diagram was prepared by the Illustrator for Biological Sequences (IBS) software (Liu et al., 2015).