Plant glutathione transferases
© BioMed Central Ltd 2002
Published: 26 February 2002
The soluble glutathione transferases (GSTs, EC 126.96.36.199) are encoded by a large and diverse gene family in plants, which can be divided on the basis of sequence identity into the phi, tau, theta, zeta and lambda classes. The theta and zeta GSTs have counterparts in animals but the other classes are plant-specific and form the focus of this article. The genome of Arabidopsis thaliana contains 48 GST genes, with the tau and phi classes being the most numerous. The GST proteins have evolved by gene duplication to perform a range of functional roles using the tripeptide glutathione (GSH) as a cosubstrate or coenzyme. GSTs are predominantly expressed in the cytosol, where their GSH-dependent catalytic functions include the conjugation and resulting detoxification of herbicides, the reduction of organic hydroperoxides formed during oxidative stress and the isomerization of maleylacetoacetate to fumarylacetoacetate, a key step in the catabolism of tyrosine. GSTs also have non-catalytic roles, binding flavonoid natural products in the cytosol prior to their deposition in the vacuole. Recent studies have also implicated GSTs as components of ultraviolet-inducible cell signaling pathways and as potential regulators of apoptosis. Although sequence diversification has produced GSTs with multiple functions, the structure of these proteins has been highly conserved. The GSTs thus represent an excellent example of how protein families can diversify to fulfill multiple functions while conserving form and structure.
Gene organization and evolutionary history
Glutathione transferases (GSTs; EC 188.8.131.52) are soluble proteins with typical molecular masses of around 50 kDa, and each is composed of two polypeptide subunits. Classically, GSTs catalyze the transfer of the tripeptide glutathione (γ-glutamyl-cysteinyl-glycine; GSH) to a cosubstrate (R-X) containing a reactive electrophilic center to form a polar S-glutathionylated reaction product (R-SG). These enzymes were first discovered in animals in the 1960s as a result of their importance in the metabolism and detoxification of drugs . Their presence in plants was first recognized shortly afterwards in 1970, when a GST activity from maize was shown to be responsible for conjugating the chloro-S-triazine atrazine with GSH, thereby protecting the crop from injury by this herbicide . Since that time, GST activities, or the corresponding enzymes or gene sequences, have been identified in all animals, plants and fungi analyzed to date [1,3]. In addition to the dimeric soluble GSTs, other proteins have been identified as having a restricted ability to conjugate xenobiotics (foreign organic compounds) with GSH, notably the distantly related mitochondrial kappa GSTs and the trimeric microsomal GSTs of animals [4,5]. These GSTs will not be considered further in this article.
Following the purification and cloning of GSTs active in herbicide detoxification in maize in the 1980s , it quickly became apparent that the plant enzymes differed significantly in sequence from their mammalian counterparts . Since that time, a large number of GSTs and GST-like sequences have been cloned from a variety of plants, and in order to make sense of this plethora of genes, a classification system was set up, at first with just three classes, theta, tau and zeta . As our understanding of GST gene families in plants and animals has expanded, this original classification system has had to be refined. To best understand the organization of GSTs in higher plants we can now take advantage of the full genome sequence of Arabidopsis thaliana.
From predicted amino-acid sequence, the soluble dimeric GSTs of Arabidopsis may be grouped into four classes. Extending the accepted nomenclature used in the mammalian GSTs, these are termed the phi, zeta, tau and theta classes (Figure 1). Phylogenetic analysis would suggest that all soluble GSTs have arisen from an ancient progenitor gene. Zeta and theta GSTs are found in both animals and plants, but the tau and phi classes are plant-specific. Searches for GST-like sequences in the Arabidopsis genome identify a further two genes related to soluble GSTs (EMBL AL132970, gene T15C9_60 and EMBL AL162973, gene F9G14_100; our unpublished data). These genes have clearly evolved from a GST progenitor and are known to be co-induced with phi and tau GSTs in cereals following exposure to herbicide safeners, chemicals that increase tolerance to herbicides . We have termed these GST-like genes lambda GSTs.
From the size and sequence diversity within the GST superfamily in Arabidopsis, it is clear that there is scope for considerable functional diversification; analysis of expressed sequence tag (EST) databases shows that 41 out of the 48 GST genes are expressed (Felix Mauch, personal communication). It is also probable that several GSTs have overlapping functions, effectively leading to some redundancy. Although genome information is not yet available in the public domain for other plants, analyses of large-scale EST projects in major crops provides valuable additional information on the relative diversity of the GST gene family in plants. In maize, 12 phi, 28 tau and 2 zeta GST sequences were reported, while in soybean, 20 tau, 1 zeta and 4 phi GSTs were identified . The relative abundance of the GSTs from each class in these EST studies is broadly similar to the gene distribution determined in the Arabidopsis genome, although some plants, such as soybean, may contain a smaller complement of phi GSTs than maize or Arabidopsis.
Classification and nomenclature
Characteristic structural features
Each soluble GST is a dimer of approximately 26 kDa subunits, typically forming a hydrophobic 50 kDa protein with an isoelectric point in the pH range 4-5. In the case of phi and tau GSTs, only subunits from the same class will dimerize [15,16]. Within a class, however, the subunits can dimerize even if they are quite different in amino-acid sequence . As determined for the GSTs active in herbicide metabolism in maize and wheat, the ability to form heterodimers greatly increases the diversity of the GSTs in planta , but the functional significance of this mixing and matching of subunits has yet to be determined.
The subunits that make up the dimer are related by two-fold symmetry as shown in Figure 5b. The dimer interface is large, with a buried surface area of between 2,700 and 3,400 Å2. Most classes of GST have one of two types of subunit interface, either a hydrophobic ball-and-socket interface (alpha, mu, pi, and phi classes; as illustrated in Figure 5), or a hydrophilic interface (theta, sigma and beta classes) . Subunits from different classes of GST are not able to dimerize because of the incompatibility of the interfacial residues. As the active sites of each subunit are normally catalytically independent, the reasons that all classes of active soluble GSTs described so far are dimers, rather than monomers, remain unclear.
Localization and function
Location and regulation
Biochemical and immunological investigations point to a largely cytosolic localization for soluble GSTs in plants [14,22]. This is borne out by genomic analysis of the Arabidopsis GSTs: only one phi GST and one lambda GST show evidence of subcellular targeting to the plastid or mitochondria, and all the other GSTs contain no putative targeting sequence and would be anticipated to be in the cytoplasm. There is a limited number of accounts reporting expression of specific GSTs in the nucleus as well as extracellularly, however .
Although it has been known for some time that GSTs in major cereal crops are very highly expressed, representing up to 2% of the total protein in the foliage, relatively few studies have addressed their tissue-specific expression in plants. In one study carried out in in-bred maize lines, different GST isoenzymes were seen to be expressed in different tissues . Pollen, for example, contained a single GST, whereas the scutellum contained five distinct isoenzymes. Similar specific patterns of GST expression are suggested by EST analyses of cDNA libraries prepared from the differing parts of maize plants . Tissue-specific expression can be overridden by exposing plants to chemical treatments: maize (Zea mays) ZmGSTF2, for example, is normally expressed only in the roots, appearing in the foliage only after exposure to herbicide safeners or chemical treatments . Similar patterns of expression have been determined using the promoter of a soybean tau GST to drive the β-glucuronidase reporter gene in transgenic tobacco .
The inducibility of phi and tau GSTs following exposure of plants to biotic and abiotic stresses is a characteristic feature of these genes, and many plant GSTs have been cloned by screening for cDNAs corresponding to stress-induced transcripts using differential or subtractive screening methods . Several tau GSTs are known to be strongly induced during cell division or when plants are exposed to auxin or cytokinin plant hormones [22,26]. In the course of biotic stress, both tau and phi GSTs are known to be induced by infection or by treatments that invoke plant defense reactions, as well as by osmotic stress and extreme temperatures . In some instances it seems likely that GSTs are induced by the general oxidative stress caused by these diverse treatments, but in other cases GST induction is specific to the particular stress . Expression of GSTs is also enhanced following exposure to a range of xenobiotics: again, GSTs may be induced in response to the general cellular injury and oxidative stress caused by herbicides and chemical toxins . Other chemicals can induce the expression of specific phi and tau GSTs without imposing any discernible chemical stress on the plant, however. The best example of this is seen in cereals treated with herbicide safeners, chemicals that enhance herbicide tolerance by increasing the expression of detoxifying enzymes, including a subset of GSTs .
From what is known of the regulation of GSTs in response to biotic stress and chemical treatments, it would be anticipated that their expression is regulated predominantly at the level of transcription [22,28]. In some instances, stress treatments can give rise to new GST variants through alternative splicing, though the significance of this is not clear . The transcriptional regulation of individual subunits ultimately influences the range of GST homodimers and heterodimers formed. For example, under constitutive conditions, the dominant GSTs in the foliage of maize and wheat are the tau TaGSTU1-1 and phi ZmGSTF1-1 homodimers, respectively [24,30]. Following treatment with herbicide safeners there is an increased synthesis of specific subunits and novel heterodimers are observed [24,30]. In maize, safeners induce the synthesis of the ZmGSTF2 subunit, which then associates with the constitutively expressed ZmGSTF1 subunit to form the ZmGSTF1-2 heterodimer, one of the major GST isoenzymes in safener-treated tissue . In wheat, the three tau GST subunits, TaGSTU2, TaGSTU3 and TaGSTU4, are induced by safeners and this results in their dimerization with the constitutively produced TaGSTU1 subunit to form the TaGSTU1-2, TaGSTU1-3 and TaGSTU1-4 heterodimers, respectively . Current evidence would suggest that the relative abundance of the safener-induced heterodimers is regulated primarily by the relative abundance of newly synthesized subunits.
The idea that GSTs have additional functions not directly derived from their ability to catalyze the formation of GSH conjugates has gained further ground with studies demonstrating that several stress-inducible GSTs protect plants from oxidative injury by functioning as glutathione peroxidases [32,33]. Certain theta, phi and tau GSTs have been shown to have glutathione peroxidase activity, with the GSTs using glutathione to reduce organic hydroperoxides of fatty acids and nucleic acids to the corresponding monohydroxyalcohols (Figure 6c). This reduction plays a pivotal role in preventing the degradation of organic hydroperoxides to cytotoxic aldehyde derivatives. This functionality in GSTs has been demonstrated to be important in tolerance of transgenic tobacco to chilling and salt  and in herbicide cross-resistance in black-grass . Interestingly, a further link between GSTs and oxidative-stress tolerance has been established by the finding that when expressed in yeast, a tau GST from tomato can suppress apoptosis induced by the Bax protein , apparently by preventing oxidative damage (Figure 6d). GSTs may also function in stress tolerance through a role in cell signaling (Figure 6e), following the observation that the induction of the genes encoding enzymes of flavonoid biosynthesis in parsley by ultraviolet light requires GSH and the expression of a specific tau GST . A further catalytic role that does not involve GSH conjugation has been demonstrated for the zeta GSTs. The Arabidopsis zeta GST catalyzes the GSH-dependent isomerization of maleylacetoacetate to fumarylacetoacetate (Figure 6f), the penultimate step in tyrosine degradation .
From a consideration of the way in which plant GSTs have adapted to fulfill a diverse range of functions, it is of interest to study the enzyme chemistry of the GSTs. The conserved nature of the G site suggests that the binding and correct orientation of glutathione is of central importance. The G site also facilitates the ionization of the sulphydryl group of GSH to yield the highly reactive thiolate anion through hydrogen bonding with an adjacent hydroxyl group. In mammalian alpha, pi and mu GSTs a tyrosine residue performs this function, whereas in all the plant enzymes this residue is replaced with a serine. For example, in ZmGSTF1-1 the effect of this hydrogen-bonding activation is to lower the dissociation constant (pKa) of the thiol from 8.7 to 6.2 . In contrast, the beta GSTs have a cysteine in place of the serine/tyrosine residue; this promotes the formation of mixed disulphides with GSH, resulting in a very different catalytic activity from that of the other GSTs. The more variable H site is responsible for accepting a wide range of hydrophobic cosubstrates of diverse chemistries, with the powerful thiolate anion then driving a range of reactions. From what is known of the enzyme kinetics of the glutathione conjugation of model xenobiotic substrates, the reactions would be anticipated to undergo a random sequential two-substrate, two-product mechanism with the overall reaction rate being determined by the rate of release of reaction product from the active site .
The plant GST family presents a conundrum for functional genomics. The genome and EST databases have allowed us to classify GSTs and study their evolution and sequence diversity, while crystallographic studies have provided powerful insights into their structural biology. The challenge remains, however: what are the functions of these proteins, where are they located and why are they so numerous and subject to such complex regulation? GSTs appear to have many different functions in plants in primary and secondary metabolism, stress tolerance and cell signaling. From complementation studies , it is also probable that quite dissimilar GSTs share similar functions. Addressing these issues is now the main challenge for GST functional genomics, and continued analysis of this protein superfamily will no doubt reveal many other examples of their functional diversification.
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