| Glutathione S-transferase: an enzyme for chemical defense in plants |
Decio Karam, Brazilian Agricultural Research Corporation (EMBRAPA)
Chemical defenses in plants can be classified in two distinct groups: constitutive and induced defenses. Glutathione (GSH) a tripeptide (-L-glutamyl- L-cisteinyl-glycine, first reported in 1988 as a philothion, distributed in the intracellular space of plants, animals, and microorganisms has two general functions: to remove toxic metabolites from the cell and to maintain cellular sulfhydril groups in their reduced form. Glutathione (GSTs: EC 184.108.40.206) are enzymes that detoxify endobiotic and xenobiotic compounds by covalent linking of glutathione to hydrophobic substrate. GST enzymes have been identified and characterized in insects, bacteria, and in many plant species. Plant glutathione s-transferase shows three groups based on the phylogenetic tree and genetic distance. There is evidence that maize GST has a small region of high amino acid sequence identify with mammalian alpha, mu, and pi class GST subunits. These classes are present only in animals and yeasts and not present in bacteria and plants. Herbicide detoxification by glutathione s-transferase has been widely studied. Maize seedling GST activities was classified in the order alachlor ( fluorodifen ( atrazine ( metolachlor. GST activity sequence observed for atrazine was Zea mays ( P. miliaceum (( S. bicolor = S. faberi = D. sanguinalis = Abutilon theophrasti ( E. crus-galli. Although little is known about other biological GST functions, there is some evidences that GST also may be induced by heavy pathogen attack and heavy metals. Gst1, induced by pathogen attack, presents in wheat showed similarity to with maize GST. Maize glutathione s- transferase Bronze2 (Bz2) is induced by cadmium treatment. A review of the glutathione s-transferase importance for detoxification in plants is presented.
Plants and other organisms have developed mechanisms to defend themselves against herbivores, insects, pathogens, or chemical compounds that are harmful to their survival. These strategies have been classified in two distinct groups: constitutive and induced defenses. Constitutive defenses also referred to as "natural" or "innate" resistance provide natural protection while induced defenses are created by an external agent such as an insect, pathogen, or xenobiotic. One induced mechanism is activation of specific enzymes that inactivate chemical compounds or detoxify heavy metals in plants.
Glutathione ((-L-glutamyl-L-cisteinyl-glycine), a submajor constituent of all cells and almost always the major nonprotein thiol compound present in cells, was first reported in 1888 by De Rey-Pailhade as a philothion (RH2) and shown to be responsible for formation of hydrogen sulfide when yeast cells were crushed with elemental sulfur. He also reported that philothion were present in beef muscle, beef liver, sheep brain, lamb small intestine, fish muscle, egg white, fresh sheep blood, and in freshly picked asparagus tips. Hopkins renamed philothion in 1921 as glutathione (Boyland and Chasseaud 1969; Meister 1989). Glutathione (GSH) shows two peptide bounds, two carboxylic acid groups, one amino group, and one thiol group (Fig. 1).
Fig. 1. Chemical structure of glutathione. The high number of hydrophilic functional groups in glutathione combined with its low molecular weight leads to high water solubility (Kosower 1976). Glutathione that is distributed in the intracellular space of plants, animals, and microorganisms has two general functions: to remove toxic metabolites from the cell and to maintain cellular sulfhydril groups in their reduced form (Liebman and Greenberg 1988). Glutathione metabolism involves many reactions (Fig. 2) where glutathione is synthesized, degraded, conjugated or oxidized. In one of these pathways, the glutathione S-transferase (GSTs, E.C.220.127.116.11), a family of multifunctional isozymes in vertebrates, plants, insects and aerobic microorganisms (Armstrong 1993), catalyzes both GSH-dependent conjugation and reduction (Ketterer et al. 1993).
Fig. 2. Description of the metabolism of glutathione with all pathways possible. 1 (-glutamylcysteine synthetase; 2 GSH synthetase; 3 (-glutamyltranspeptidase; 4 dipeptiddases; 5 (-glutamylcyclotransferase; 6 5-oxoprolinase; 7 GSH s- transferase; 8 N-acethyltransferase; 9 GSH peroxidases; 10 GSH thiol transferases; 11 reaction of free radicals with GSH; 12 gluthatione disulfide (GSSG) reductase; 13 transport of (-Glu-(Cys)2 (Meister 1989).
Glutathione s-transferase detoxifies endobiotic and xenobiotic compounds by covalently linking glutathione to a hydrophobic substrate, forming less reactive and more polar gluatathione s-conjugate (Neuefeind et al. 1997). Glutathione S- transferases are dimeric enzymes that show five independent classes, alpha, mu, pi, sigma (Buetler and Eaton 1992; Drogg et al. 1995; Ketterer et al. 1993; Neuefiend 1997), and theta (Buetler and Eaton 1992; Drogg et al. 1995; Neuefiend 1997). Classes alpha, mu and pi initially proposed by Mannervick et al. in 1988 (Buetler and Eaton 1992), are presents only in animals and yeasts but absent in bacteria and plants (Pemble and Taylor 1992). The very heterogeneous theta class, reported by Meyer et al 1991 (Buetler and Eaton 1992) are presents in yeasts, plants, bacteria, rats, humans, chickens, salmon, and non veterbrates such as flies and apparently absent in lower animals such as molluscs, nematodes, and platyhelminthes (Taylor et al 1993). Buetler and Eaton in 1992 assembled a database of 71 full length and near full length amino acid sequences of glutathione s-transferases from various vertebrates, eukaryotes and prokaryotes. With this database they established a dendrogram identifying classes alpha, mu, pi, theta, and sigma.
Detoxification of chemical compounds
Detoxification in plants is a process (Fig. 3) tat metabolizes foreign compounds. It can be separated into two sequential processes: chemical (modification) transformation, and compartmentation. These two processes are divided into three phases: phase I (activation) reactions, phase II (conjugation), and phase III (internal compartmentation and storage processes) (Coleman 1997; Marrs 1996; Sabnderman 1992).
Phase I usually involves hydrolysis catalyzed by esterases and amidases or oxidation catalyzed by the cytochrome P-450 system. Phase II involves the deactivation synthesis of xenobiotic or a phase I-activated metabolite by covalent linkage to an endogenous hydrophilic molecule, such as glucose, malonate or glutathione resulting in a nontoxic or less toxic compound. Phase II is catalyzed by glucosyl-, malonyl, or glutathione transferases. In phase III, the inactive water soluble conjugates formed in phase II, are exported from the cytosol by membrane-located proteins, which initiate the compartmentalization and storage in the vacuole (soluble conjugates) or in the cell wall (insoluble conjugates) (Coleman 1997; Marrs 1996; Sabnderman, 1992).
Fig. 3. Detoxification process of xenobiotics in plants. Broken arrows represent a proposed patway for the glucosylation of xenobiotics in the Golgi, followed by release of the metabolites into the apoplast. CT, glutathione-conjugate transporte; AT, ATP-dependent xenobiotic anion (taurocholate) transporter; GT, ATP-dependent glucoside-conjugate transporter; VP, vacuolar peptidase (Coleman et al., 1997).
Glutathione s-transferase in plantsGlutathione s-transferase in plants
Glutathione s-transferases (GST), first discovered because of their ability to metabolize toxic exogenous compounds, have been identified and characterized in insects (Harold and Ottea 1997), in bacteria (Zablotowich et al. 1995), and in many plants such as maize (Edwards and Owen 1986; Rossini et al. 1996; Jablonkai and Hatzios 1991; Scarponi et al. 1992; Jepson et al. 1994; Holt et al. 1995; Marrs et al. 1995; Hatton et al. 1996; Dixon et al. 1997; Marrs and Walbot 1997), wheat (Jablonkai and Hatzios 1991; Mauch and Dudler 1993, Romano et al. 1993; Edwards and Cole 1996; Riechers et al. 1996; Riechers et al. 1997), tobacco (Droog et al. 1995), dwarf pine (Schroder and Rennenberg 1992), soybean (Ulmasov et al. 1995; Andrews et al. 1997), Arabidopsis thaliana (Reinemer et al. 1996), barley (Romano et al. 1993; Wolf et al. 1996), Setaria spp. (Wang and Dekker 1995), carnation (Meyer et al. 1991), potato (Hahn and Strittmatter 1994), chickpea (Hunatti and Ali 1990, 1991), sorghum (Gronwald et al. 1987; Dean et al. 1990), velvetleaf (Anderson and Gronwald 1991) and sugarcane (Singhal et al. 1991). According to Lamoureux and Rusness (1993) cited by Marrs (1996) there are over 33 plant species with GST activity, although in many cases the GSTs have been not purified. Drogg et al. (1995) proposed three categories of glutathione s-transferase in plants, type I, II, and III (Fig. 4), based on the phylogenetic tree and genetic distance obtained in the evolutionary relationship between 16 plant GST protein sequences available. Type I contains three exons and two introns, type II contains ten exons and nine introns, and type III contains two exons and one intron (Marrs 1996). Plant glutathione s- transferases are comparable to theta class, although type II also corresponds in sequence and intron position to alpha class GST in mammalian. Taylor et al (1987) cited by Taylor et al (1993) show evidence that maize GST has a small region of high amino acid sequence same as with mammalian alpha, mu, and pi class GST subunits.
Fig. 4. Phylogenetic tree of plant type I, II, and III glutathione s-transferase obtained from Genbank or PIR (Marrs, 1996).
Type I GST includes GST I, GST II, GST III, and GST IV present in maize that show substrate specificity toward herbicides such as alachlor, atrazine, or metolachlor. Other GSTs classified in this group are GstA (gene) cDNA WIR56 in wheat, parB (gene) in tobacco, PMA239X14, AW124, gst2/Atpm24, ERD11, and ERD13 in Arabidopsis thaliana. Type I GST was also cloned from broccoli, sugarcane, Silene cucubalis, and Hyoscyamus muticus. Type II is represented only by GST1 (pSR8) and GST2 from carnation whose substrate specificity is unknown although there is speculation that they participate in lipid peroxidation. Type III consist of GmHsp26A or GHT2 in soybeans, prp1-1 (gene) also called Gst1 from potato, parA/Nt114, parC/Nt107, Nt103, and Nicotina plumbaginfolia msr1 (pLS216) from tobacco, bronze -2 from maize, and GST5 from Arabidopsis thaliana, first identified as a set of homologous genes, is induced toward auxin, ethylene, pathogen infection, heavy metals, and heat shock. Another glutathione s-transferases such as Sorghum GSTs 1-6, GST I, II, III, IV from chickpea, soluble (37kD), soluble (47 kD), and microsomal from pea, GST25 and GST26 from wheat, GST1 from Arabidopsis thaliana, GST I and GST II from Picea abies, Zea mays (function as 30 kD monomer) from maize, and Phaseolus vulgaris from French bean have been characterized, but because of the amino acid sequence still unavailable impeding grouping in classes I, II, and III (Marrs, 1996).
Herbicide detoxification in plants
Mortimer (1997) discussed the possibility of phenological adaptation in weeds in terms of an evolved response to herbicides, however this phenological adaptation remains largely unexplored. On the other hands one basis for selectivity is the fact that plants can detoxify some herbicides fast enough to avoid accumulation to phytotoxic levels. Herbiicides, usually highly lipophilic, metabolized by enzymatic reactions change reactivity and polarity. These compounds are eliminated by conjugation, detoxification, deposition, and so on, more rapidly than they are replenished (Devine et al. 1993). The basic reaction of herbicide detoxification is oxidation, reduction, hydrolysis, and conjugation (Duke 1985). A much less phytotoxic product is created or in many cases the product is inactive (Cole 1994). Glutathione s-transferase is one enzyme that participates in herbicide detoxification. A very important conjugation in plant herbicide metabolism is the thiol reaction attack of the GSH to an eletrophilic substrate with a displacement of a nucleophile (Fig. 5) (Armstrong 1993; Kreuz et al. 1996). These reactions usually are catalyzed by glutathione s-transferase as first reported by Lamourex et al. (1970) in maize with conjugation of glutathione and atrazine (Kreuz et al. 1996).
R-X + GST (r) R-SG + HX
Fig. 5. Generic reaction, atrazine, tridiphane, EPTC, fluorodifen, and aciflurofen reaction catalyzed by glutathione s-transferase.
Several GSTs have been characterized in maize such as GST I, a homodimer of 29kDa subunits, GST II, a heterodimer of 27 kDa and 29 kDa subunits, GST III, a homodimer of 26kDa subunits, and GST IV, a homodimer of 27kDa subunits. GST I and GST II comprise 1 to 2% of the soluble protein in maize. GST 27 present in both GST II and IV were present in RNA isolated from maize root but expression was not detected in RNA from aerial parts of the plant. GST 29 was expressed in the stem and leaves and to lower levels in pollen and endosperm. GST 27 besides play a role in isoforms which are not only involved in detoxification of xenobiotics but also catalyze the conjugation of glutathione to endogenous substrates (Jepson et al. 1994)
GST activity present in cultured cells to the enzyme extracted from maize cultivars resistant to s-triazine herbicides was compared. Precipitates of crude enzyme extracts from maize showed activity 0.04, 0.08, 0.09, and 0.002 mol product/mg protein min, respectively for cv. DeKalb leaves, cv. Fronica leaves, cv. LG11 leaves, and Black Mexican Sweet Corn suspension culture harvested 7 days after incubation (DAI). When atrazine was used as a substrate, GSH conjugation rate catalyzed by glutathione s-transferase was very low at all suspension culture harvests. GST activity varied from 1.3 to 3.2 mol product/mg protein min. when metolachlor was used as a substrate. Leaf GST activity in atrazine substrate was 0.022 (7 DAI), 0.022 (10 DAI), and 0.015 (14 DAI) mol product/g fresh weight cells min, and 9.3 (4 DAI), 17.1 (7 DAI), 10.6 (10 DAI), and 11.4 (14 DAI) mol product/g fresh weight cells min when metolachlor was used as a substrate (Edwards and Owen 1986).
Hatton et al. (1996) characterized the glutathione dependent herbicide- detoxification system in maize and in associated weeds, by determining GST activities. In saturating substrate concentrations, maize seedlings contained GST activities toward differing classes of substrates was classified in the order alachlor ( fluorodifen ( atrazine ( metolachlor. The same activity sequence was obtained by Digitaria sanguinalis, Echinochloa crus-galli, Panicum miliaceum, Setaria faberi, and Sorghum bicolor. The GST activity sequence observed for atrazine was Zea mays ( P. miliaceum (( S. bicolor = S. faberi = D. sanguinalis = Abutilon theophrasti ( E. crus-galli. Their results establish a good correlation between the relative GSH specific activity toward alachlor and an excellent correlation with metolachlor.
All GST activity of maize cv. Pioneer 3394 and Artus were higher in roots than shoots toward alachlor, metolachlor, and fluorodifen while shoots showed higher GST activity toward atrazine. In shoots without the herbicide-safener dichlormid, GST activity observed was atrazine = alachlor = metolachlor ( fluorodifen. When shoots where treated with dichlormid, GST activity increased for all herbicides. The highest GST root activity was observed toward the chloroacetanilides increased in Pioneer 3394 when safener was used (Dixon et al 1997).
Jablonkai and Hatzios (1991) studied the role of shoot and root glutahione and glutathione s-transferase activity in response of two maize hybrids and one wheat cultivar to acetochlor, a chloroacetanilide herbicide. GST activity showed a strong dependence on acetochlor concentration. GSH/acetochlor ratio at lower acetochlor concentrations was high, corresponding to higher acetochlor conjugate formeatiion. Root GST activity in both hybrids was greater and more inducible by acetochlor pretreatment than in susceptible wheat.
Analysis for characterization of glutathione s-transferase isoforms in maize showed that susceptible and intermediate lines exhibited impaired functions of GST-27 and GST-29 subunits, respectively. GST IV appears to be the principal detoxifying enzyme for alachlor, although GST I and II are required to achieve tolerance to high rates of alachlor (Rossini et al. 1996).
Glutathione s-transferase was purified from maize roots treated with safeners, GST II and GST I. GST II, a heterodimer of 29 and 27-kDa subunits, was present in untreated seedling roots and absent in other maize organs. GST II seedling root activity varied from 20 to 40% in untreated seedling roots but in roots treated with safeners, GST II enzymatic activity increased to 45% of the total seedling root GST activity. GST II was about seven times more active against alachlor than GST I . GST 29, common in GST I and GST II, was present in all treated and untreated maize organs with safeners while GST 27 was found only in untreated maize organs at low levels. GST 27 was induced in all the major aerial organs (Holt et al. 1995).
Although piperonyl butoxide (PBO) was reported to increase the herbicidal activity of triazines in various plants, Varsano et al. (1992) observed that atrazine conjugation with GSH, catalyzed by GST, in maize was not inhibited by PBO. This was assumed to be due to cellular level action. PBO inhibition of GST was rather limited and did not explain the observed synergistic effect of PBO and atrazine.
Ezra and Stephenson (1985) found that proso millet (Panicum miliaceum) roots had about 50% of the GSH of corn roots. Proso millet shoot showed less than 10% the GST activity of proso millet roots equivalent to 33% of the corn root enzyme. Shoot enzymatic activity in proso millet is equivalent as 10% of the corn shoot enzyme. Glutathione concentration was 35.9 and 65.4 (g GSH/ g fresh weight for proso millet root and corn root, respectively. Safener R-25788 elevated GSH activity to 62.7 but not increased proso millet GST activity. The difference observed in tolerances to atrazine and EPTC between corn and proso millet was related to the different rate of metabolism of the herbicide by proso millet.
The effect of herbicide antidotes on the glutathione s-transferase of etiolated Sorghum bicolor shoot was investigated by Dean et al. (1990). Untreated seedlings showed two distinct GSTs, a major (GST-1) with activity toward CDNB (1-chloro-2,4-dinitrobenzene) and a minor (GST-7) toward metolachlor. Treated with various antidotes, sorghum seedlings show four to five additional GST with activity toward metolachlor and little or no activity toward CDNB. The GST (metolachlor) activity in etiolated shoots was increased 1.8 fold and 6.5 fold by 24 hour treatment with 1(M and 160(M metolachlor respectively. According to the author these results are consistent with the finding that antidotes protect sorghum against metolachlor inducing de novo synthesis of glutathione s-transferase.
Glutathione s-transferase activity in sorghum was increased less than two fold when CDNB (1-chloro-2,4-dinitrobenzene) was used as a substrate. In contrast, when metolachlor was the substrate, GST activity was increased in average 18 fold in response to antidote treatment. When metolachlor was used as a substrate, the enzymatic activity in untreated sorghum, was 0.07 nmol/mg protein hr while the enzymatic activity in treated sorghum with antidotes varied from 0.36 to 2.08 nmol/mg protein hr. The relative ability of a particular antidote to enhance GST activity was highly correlated with protection against metolachlor. The GST (metolachlor) activity in moles GSH-metolachlor conjugated/ mg protein hr relation was established as a function of shoot length (expressed in % of antidote-treated control) * 0.032 - 0.963 (Gronwald et al. 1987).
Glutathione s-transferase's contribution to herbicide detoxification and selectivity suspension in soybean, Abutilon theophrasti, Amaranthus retroflexus, Digitaria sanguinalis, Echinochloa crus-galli, Ipomoea hederacea, Setaria faberi, and Sorghum halepense was determined. For the leguminosae GST activity was determined using homoglutathione (hGSH, (-L glutamyl-L-cysteinyl-(-alanine) while for the other species GSH was used. In cultured cells of soybean, GST activity was fomesafen ( metolachlor = acifluorfen ( chlorimuron ethyl. Soybean cultured cell and 14 day old seedling showed the highest specific activity with metolachlor and fomesafen. When fomesafen was used as a substrate the order of GST activity was soybean (( E. crus-galli ( D. sanguinalis ( S. halepense = S. faberi while A. theophrasti, A. retroflexus, and I. hederacea did not show any GST activity. When metolachlor was used as a substrate the order was soybean ( A. theophrasti (( S. halepense ( A. retroflexus ( I. hederacea while E. crus-galli, D. sanguinalis , and S. faberi did not show any GST activity. The results showed correlation between the selectivity of fomesafen and the GST activity for all species studied while for metolachlor the correlation between selectivity and the GST activity was observed only toward broadleaved weeds (Andrews et al. 1997). Metolachlor accumulation in roots and shoots was greater in soybean than in corn seedlings due to a higher herbicide-induced activity of glutathione s-transferase in corn (Scarponi et al. 1992).
The most GST (atrazine) activity in Abutilon theophrasti was observed in leaf tissue while low levels were detected in stems and no activity was observed in roots. GST concentration was 5.6 fold greater in leaf tissue than in stems. In this study, there was evidence that enhanced GST activity may result in the development of herbicide resistance in weeds (Anderson and Gronwald 1991).
Bread wheat and other Triticum species contain GST activity toward fenoxaprop in roots, shoots, and unbleached plain flour. GST activity was increased with treatment of safeners. GST activity measured in 5, 7, 10, and 12 day old seedlings were 86, 80, 60, and 71 nkats/g protein for shoot and 196, 152, 113, and 100 nkats/g protein for roots respectively. When safener was used, shoot and root GST activities increased. GST activity obtained with safener treatment varied from 182 to 235 nkats/g protein for shoot and from 280 to 468 nkats/g protein for roots. GST detoxification of fenoxaprop in wheat is in contrast to the metabolic fate of the diclofop that is hydroxylated by the cytochrome P450. The GST activity responsible for fenoxaprop detoxification was 10 fold lower toward fenoxaprop-ethyl suggesting that the herbicide requires ester hydrolysis to create rapid detoxification by glutathione conjugation (Edwards and Cole 1996).
Glutathione s-transferase levels in wheat shoots and wheat shoot relatives with and without safeners were quantified (Riechers et al. 1996). Maize GST antibody indicated presence of GST activity in untreated wheat and wheat relatives with safener enzymatic levels increased to a similar extent. On the other hand GST dimethenamid assay determined little or no constitutive GST dimethenamid activity. The GST dimethenamid activity also was increased with safener treatment. GST dimethenamid activity varied from ND (not detectable) to 107 pmol/mg protein*min in approximately 58 wheat line (Fig. 6).
Fig 6. Glutathione s-transferase dimethenamid activity in crude extracts of wheat and wheat relatives (Riechers et al. 1996).
Glutathione s-transferase in pathogen defenses
Although plant glutathione s-transferase has been largely studied with regard to its role in herbicide detoxification, little is known about other biological functions of GST in plants. Evidence that pathogen attack results in an effective increase of mRNa coding a protein homologous to glutathione s- transferase was presented by Dubler et al. (1991) for wheat. Mauch and Dubler (1993) characterized a pathogen-induced gene from wheat that was called GstA1 based on sequence similarity showed with maize glutathione s-transferase. GstA1 was expressed at a low basal level in healthy control plants. GstA1 level increased drastically and remained elevated for two days after plant inoculation with Erysiphe graminis f. sp. hordei and E. g. f. sp. tritici. The result observed indicated that the GstA1 expression is generally in response to infection. This was supported by GstA1 induction by Puccinia recondita f. sp. tritici, another fungal pathogen. One member of the prp1 gene family responsive to pathogen, ppr1-1 that encodes a cytosolic glutathione s-transferase from potato increased upon infection with Phytophthora infestans (Hahn and Strittmater 1994).
Glutathione s-transferase induced by heavy metals
Plants have mechanisms that maintain essential metal concentrations between deficient and toxic limits as well as mechanisms to keep nonessential metals at low toxicity thresholds (Rauser 1995). Plant glutathione s-transferase also may be induced by heavy metals, wounding, ethylene, and ozone to generate an active oxygen species (Fig 7) during oxidative stress. (Marrs 1996).
Maize seedlings were incubated in solutions of plant hormones, sodium chloride, cobalt chloride, cadmium chloride, and sodium arsenite or placed under environmental stress conditions (cold, hypoxia - flooding roots with water, and heat shock). Cadmium induced strongly maize glutathione s-transferase Bronze2 (Bz2) and GST III. Salt stress, hypoxia, and heat shock had no effect on Bz2, whereas plant hormone, cold, and arsenite induced Bz2 transcript accumulation. As a result of cadmium treatment spliced Bz2 increase 20 fold and unspliced Bz2 increased more than 50 fold over the levels of unspliced Bz2 Rna in control protoplasts. B37, a maize inbred line was the only one that showed a cadmium- responsive GST activity (Marrs and Walbot 1997). Mauch and Dudler 1993 observed that wheat GST25 and GST26 activities also increased in the presence of cadmium.
Fig. 7. Active oxygen species inducing GST levels that metabolize the toxic produts of lipid peroxidation and DNA damage (Marrs 1996).
Anderson, M. P. and Grownland, J. W. 1991. Atrazine resistance in velvetleaf (Abutilon theophrasti) biotype due to enhanced glutathione s-transferase activity. Plant physiology. 96: 104-109.
Andrews, C. J., Skipsey, M., Townson, J. K., Morris, C., Jepson, I, Edwards, R. 1997. Glutathione transferase activities toward herbicides used selectively in soybean. Pesticide science. 51: 213-222.
Armstrong, R. N. (1993). Glutathione s-transferases: structure and mechanism of an archetypical detoxification enzyme. Advanced enzymology. 69: 1-44.
Boyland, E. and Chasseaud, L. F. 1969. The role of glutathione and glutathione s-transferases in mercaptuic acid biosynthesis. Advanced enzymology. 32: 173- 219.
Buetler, T. M., Eaton, D. L. 1992. Glutathione s-transferases: amino acid sequence comparison, classification and phylogenetic relationship. Journal of environmental science and health. Part C., Environmental carcinogenesis and ecotoxicology reviews. 10(2), 181-203.
Cole D. 1994. Detoxification and activation of agrochemicals in plants. Pesticide science. 42: 209-222.
Coleman, J. O. D., Mechteld, M. A., Blake-Kalff, Emyr Davis, T. G. 1997. Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends in plant science. 2: 141-151.
Dean, J. V.; Grownwald, J. W.; Eberlein, C. V. 1990. Induction of glutathione S- transferase isozymes in sorghum by herbicide antidotes. Plant Physiology. 92:467-473.
Devine, M. D.; Duke, S. O.; Featke, C. 1993. Physiology of herbicide action. PTR Prentice Hall, Englewood Cliffs, New Jersey. Dixon, D., Cole, D. J., Edwards, R. 1997. Characterization of multiple glutathione transferases containing the GST I subunit with activities toward herbicide substrates in maize (Zea mays). Pesticide science. 50: 72-82.
Drogg, F. N. J.; Hooykaas, P. J. J.; Van der Zaal, B. J. 1995. 2,4 dichlorophenoxyacetic and related chlorinated compounds inhibit two auxin- regulated type-III tobacco glutathione S-transferase. Plant Physiology. 107: 1139-1146.
Dubler, R.; Hertig, C.; Rebmann, G.; Bull, J.; Mauch, F. 1991. A pathogen- induced wheat gene encodes a protein homologous to glutathione s-transferase. Molecular plant-microbe interactions. 4(1): 14-18.
Edwards, R. and Cole, D. J. 1996. Glutathione transferase in wheat (Triticum) species with activity toward fenoxaprop-ethyl and other herbicides. Pesticide Biochemistry and Physiology. 54: 96-104.
Edwards, R. and Owen, W. J. 1986. Comparison of glutathione s-transferases of Zea mays responsible for herbicide detoxification in plants and suspension- cultured cells. Planta. 169: 208-215.
Ezra and, G. and Stephenson, G. R. 1985. Caomparative meatbolism of atrazine and EPTC in proso millet (Panicum miliaceum L.) and corn. Pesticide biochemistry and physiology. 24: 207-212.
Grownland, J. W., Fuerst, E. P., Eberlein, C. V., Egli, M. A. 1987. Effect of herbicide antidotes on glutathione content and glutathione s-transferase activity of shorgum shoots. Pesticide biochemistry and physiology. 29: 66-76.
Hahn, K. and Strittmater, G. 1994. Pathogen-defence gene prp1-1 from potato encodes an auxin-responsive glutathione s-transferase. European journal of biochemistry. FEBS 226: 619-626.
Hatton, P. J., Dixon, D., Cole, D. J., Edwards, R. 1996. Glutathione transferase activities and herbicide selectivity in maize and associated weed species. Pesticide science. 46: 267-275.
Harold, J. A. and Ottea, J. A. 1997. Toxicological significance of enzyme activities in profenofos-resistant tobacco budworms, Heliothis virescens (F.). Pesticide biochemistry and Physiology. 58: 23-33.
Holt, D. C., Lay, V. J., Clarke, E. D., Dismore, A., Jepson, I., Bright, S. W. J., Greenland, A. J. 1995. Characterization of the safener-induced glutathione s-transferase isoform II from maize. Planta. 196: 295-302.
Hunatti, A. A. and Ali, B. R. 1990. Glutathione s-transferase from oxadiazon treated chickpea. Phytochemistry. 29(8): 2431-2435.
Hunatti, A. A. and Ali, B. R. 1991. The induction of chickpea glutathione s- transferase by oxadiazon. Phytochemistry. 30(7): 2131-2134.
Jablonkai, I. and Hatzios, K. K. 1991. Role of glutathione and glutathione S- transferase in the selectivity of acetochlor in maize and wheat. Pesticide Biochemistry and Physiology. 41; 221-231.
Jepson, I., Lay, V. J., Holt, D. C., Bright, S. W. J., Greenland, A. J. 1994. Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione s-transferases isoform I, II and IV. Plant molecular biology. 26: 1855-1866.
Ketterer, B., Taylor, J., Meyer, D., Pemble, P., Coles, B., ChuLin, X., Spencer, S. 1993. Some functions of glutathione transferases. In: Structure and function of glutathione transferases, ed. Kenneth D. Tew, Cecil B. Pickett, Timothy J. Mantle, Bengt Mannervik, and John D. Hayes. CRC Press, Boca Raton, Florida. Kosower, E. M. 1976. Chemical properties of glutathione. In: Glutathione: metabolism and function, ed. Irwin M. Arias and William B. Jakoky. Raven Press, New York. Kreuz, K.; Tommasini, R.; Martinoia, E. 1996. Old enzymes for a new job: Herbicide detoxification in plants. Plant Physiology. 111: 349-353.
Liebman, J. F.; Greenberg, A. 1988. Mechanistic principles of enzyme activity, VCH Publishers, New York. Mauch, F. and Dudler, R. 1993. differential induction of distinct glutathione S-transferases of wheat by xenobiotics and by pathogens attack. Plant Physiology. 102: 1193-1201.
Marrs, K. A. 1996. The functions and regulation of glutathione s-transferases in plants. Annual review of plant physiology and Plant molecular biology. 47, 127- 158.
Marrs, K. A., Alfenito, M. R., Lloyd, A. M., Walbot, V. A. 1995. Glutathione s- transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature. 375: 397-400.
Marrs, K. A. and Walbot, V. 1997. Expression and RNA splicing of the maize glutathione S-transferase bronze2 gene is regulated by cadmium and other stresses. Plant Physiology. 113: 93-102.
Meister, A. 1989. On the biochemistry of glutathione. In: Glutathione centennial: molecular perspectives and clinical implications, ed. Naoyuki Taniguchi, Taneaki higashi, Yukiya Sakamoto, Alton Meister. Academic Press, San Diego, Ca. Meyer, R. C., Goldsbrough, P. B., Woodson, W. R. 1991. An ethylene-responsive flower senescence-related gene from carnation encodes a protein homologous to glutathione s-transferase. Plant molecular biology. 17: 227-281.
Mortimer, A. M. 1997. Phenological adaptatiion in weeds - an evolutionary response to the use of herbicides? Pesticide science. 51: 299-304.
Neuefeind, T.; Reinemer, P.; Bieseler, B. 1997. Plant glutathione S-transferases and herbicide detoxification. Biological Chemistry. 378: 199-205.
Pemble, S. E. and Taylor, J. B. 1992. An evolutionary perspective on glutathione transferases inferred from clas-theta glutathione transferase cDNA sequences. Biochemistry journal. 287: 957- .
Rauser, W. E. 1995. Phytochelatins and related peptides: structure, biosynthesis, and functions. Plant physiology. 109: 1141-1149.
Reinemer, P., Prade, L., Hof, P., Neuefeind, T., Huber, R., Zettl, R., Palme, K., Schell, J., Koelln, I., Bartunik, H. D., Bieseler, B. 1996. Three- dimensional structure of glutathione s-transferase from Arabidopsis thaliana at 2.2Å resolution: structural characterization of herbicide-conjugating plant glutathione s-transferases and a novel active site architecture. Journal of molecular biology. 255: 289-309.
Riechers, D. E., Irzyk, G. P., Jones, S. S., Fuerst, E. P. 1997. Partial characterization of glutathione s-transferase from wheat (Triticum spp.) and purification of a safener-induced glutathione s-transferase from Triticum tauschii. Plant physiology. 114: 1461-1470.
Riechers, D. E.; Yang, K.; Irzyk, G. P.; Jones, S. S.; Fuerst, E. P. 1996. Variability of glutathione S-transferase levels and dimethenamid tolerance in safener-treated wheat and wheat relatives. Pesticide Biochemistry and Physiology. 56: 88-101.
Romano, M. L., Stepheson, G. R., Tal, A., Hall, J. C. 1993. The effect of monooxygenase and glutathione s-transferase inhibitors on the metabolism of diclofop-methyl and fenoxaprop-ethyl in barley and wheat. Pesticide biochemistry and physiology. 46: 181-189.
Rossini. L.; Jepson, I.; Greenland, A. J.; Gorla, M. S. 1996. Characterization of glutathione S-tranferase isoforms in three maize inbred lines exhibiting differential sensitivity to alachlor. Plant Physiology. 112: 1595-1600.
Sandermman, H. 1992. Plant metabolism of xenobiotics. TIBS. 17: 82-84.
Scarponi, L., Alla, M. N., Martinelli. 1992. Metolachlor in corn (Zea mays) and soybean (Glycine max): persistence and biochemical signs of stress during its detoxification. Journal of agricultural and food chemistry. 40: 884-889.
Schroder, P.and Rennenberg, H. (1992) Characterization of glutathione S- transferase from dwarf pine needles (Pinus mugo Turra). Tree Physiology. 11: 151-160.
Singhal, S. S., Tiwari, N. K., Ahmad, H., Srivastava, S. K., Awasthi, Y. C. 1991. Purification and characterization of glutathione s-transferase from sugarcane leaves. Phytochemistry. 30: 1409-1414.
Taylor, J.; Pemble, S.; Harris, J; Meyer, D., Spencer, S., Xia, C.; Ketterer, B. 1993. Evolution of GTS genes. In: Structure and function of glutathione transferases, ed. K. D. Tew, C. B. Pickett, T. J. Mantle, B. Mannervik, J. D. Hayes. CRC Press, Boca Raton, Florida. Ulmasov, T., Ohmiya, A., Hagen, G., Guilfoley, T. 1995. The soybean GH2/4 gene that encodes a glutathione s-transferase has a promoter that is activated by a wide range of chemical agents. Plant physiology. 108: 919-927.
Varsano, R.; Rabinowitch, H. D.; Rubin, B. 1992. Mode of action of piperonyl butoxide as herbicide synergistic of atrazine and terbutryn in maize. Pesticide biochemistry and physiology. 44: 174-182.
Wang, R.L. and Dekker, J. 1995. Weedy adaptation in Setaria spp. III. Variation in herbicide resistance in Setaria spp. Pesticide biochemistry and physiology. 51: 99-116.
Wolf, A. E., Dietz, K. J., Schroder, P. 1996. Degradation of glutathione s- conjugates by a carboxypeptidase in the plant vacuole. FEBS letters. 384: 31-34.
Zablotowicz, R. M.; Hoagland, R. E.; Locke, M. A.; Hicley, W. J. 1995. Glutathione S-transferase activity and metabolism of glutathione conjugates by Rhizosphere bacteria. Applied and Environmental microbiology. 61(3): 1054-1060.
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