Abstract
The enzymes glutathione-S-transferases (GSTs, E.C.2.5.1.18) have been associated with detoxification of xenobiotics, limiting oxidative damage and other stress responses in plants. In this study, we report the isolation of a mustard gene, BjGSTF2, homologous to the phi class GSTs and changes in plant growth in vivo and shoot regeneration in vitro were related to GST expression. GST transcripts accumulated differentially in mustard organs, where transcript was most abundant in root. Tissues incubated at high temperature or in the presence of exogenous H2O2, HgCl2, 1-aminocyclopropane-1-carboxylate, salicylic acid and paraquat upregulated GST expression, whereas spermidine was inhibitory. To investigate the in vivo function of GST, transgenic Arabidopsis thalianaplants expressing sense (GST-S6), antisense (GST-A4) and double-stranded BjGSTF2(GST-DS1) RNAs were generated. GST-S6 was shown to flower two days earlier and was relatively more tolerant to HgCl2 and paraquat, whereas GST-DS1 with least stress tolerance flowered one week later compared to WT and GST-A4. In shoot regeneration response, tissues originated from GST-S6 were highly regenerative, whereas no shoot regeneration was observed in GST-DS1 tissues after 30 days of culture. Results of this study provide the evidence showing that GST plays a role in plant growth and development in vivo and shoot regeneration in vitro.
Similar content being viewed by others
References
M.R. Alfenito E. Souer C.D. Goodman R. Buell J. Mol V. KoesR. Walbot (1998) ArticleTitleFunctional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases Plant Cell 10 1135–1149 Occurrence Handle10.1105/tpc.10.7.1135 Occurrence Handle1:CAS:528:DyaK1cXkvFejt70%3D Occurrence Handle9668133
M.B. Amor M. Guis A. Latche M. Bouzayen J.C. Pech J.P. Roustan (1998) ArticleTitleExpression of an antisense 1-aminocyclopropane-1-carboxylate oxidase gene stimulates shoot regeneration in Cucumis melo Plant Cell Rep. 17 586–589
J.V. Anderson D.G. Davis (2004) ArticleTitleAbiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula Physiol. Plant. 120 421–433
E. Auboiron M.P. Carron N. Michaux-Feriere (1990) ArticleTitleInfluence of atmospheric gases, particularly ethylene, on somatic embryogenesis of Hevea brasiliensis Plant Cell Tissue Organ Cult. 21 31–37
N.L. Biddington R.A. Sutherland H.T. Robinson (1988) ArticleTitleSilver nitrate increases embryo production in anther culture of Brussels sprouts Ann. Bot. 62 181–185
J. Bilang H. Macdonald P.J. King A. Sturm (1993) ArticleTitleA soluble auxin-binding protein from Hyoscyamus muticus is a glutathione S-transferase Plant Physiol. 102 29–34
W. Bors C. Langebartels C. Michel H.J. Sanderman (1989) ArticleTitlePolyamines as radical scavengers and protectants against ozone damage Phytochemistry 28 1589–1595 Occurrence Handle10.1016/S0031-9422(00)97805-1 Occurrence Handle1:CAS:528:DyaL1MXkslalu74%3D
W. Chen G. Chao K.B. Singh (1996) ArticleTitleThe promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites Plant J. 10 955–966
Z. Chen H. Silva D.F. Klessig (1993) ArticleTitleActive oxygen species in the induction of plant systemic acquired resistance by salicylic acid Science 262 1883–1886 Occurrence Handle1:CAS:528:DyaK2cXhtVWqu7o%3D Occurrence Handle8266079
G.L. Chi D.G. Barfield G.E. Sim E.C. Pua (1990) ArticleTitleEffect of AgNO3 and aminoethoxyvinylglycine on in vitro shoot and root organogenesis from seedling explants of recalcitrant Brassica genotypes Plant Cell Rep. 9 195–198
G.L. Chi E.C. Pua C.J. Goh (1991) ArticleTitleRole of ethylene on de novo shoot regeneration from cotyledonary explants of Brassica campestris ssp. pekinensis (Lour) Olsson in vitro Plant Physiol. 96 178–183
C.-F. Chuang E.M. Meyerowitz (2000) ArticleTitleSpecific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 97 4985–4990
S.J. Clough A.F. Bent (1998) ArticleTitleFloral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 735–743
K. Cui G. Xing X. Liu G. Xing Y. Wang (1999) ArticleTitleEffect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum Plant Sci. 146 6–16
I. Cummins D.J. Cole R. Edwards (1999) ArticleTitleA role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass Plant J. 18 285–292
D.P. Dixon D.J. Cole R. Edwards (1998) ArticleTitlePurification, regulation and cloning of a glutathione transferase (GST) from maize resembling the auxin-inducible type-III GSTs Plant Mol. Biol. 36 75–87
D.P. Dixon B.G. Davis R. Edwards (2002) ArticleTitleFunctional divergence in the glutathione transferase superfamily in plants J Biol. Chem. 277 30859–30869
G. Drolet E.B. Dumbroff R. Legg J.E. Thompson (1986) ArticleTitleRadical scavenging properties of polyamines Phytochemistry 25 367–371
R. Edwards D.P. Dixon V. Walbot (2000) ArticleTitlePlant glutathione S-transferases: enzymes with multiple functions in sickness and in health Trends Plant Sci. 5 193–198
B. Ezaki M. Suzuki H. Motoda M. Kawamura S. Nakashima H. Matsumoto (2004) ArticleTitleMechanism of gene expression of Arabidopsis glutathione S-transferase, ATGST1, and AtGST11in response to aluminum stress Plant Physiol. 134 1672–1682
B. Ezaki Y. Yamamoto H. Matsumoto (1995) ArticleTitleCloning and sequencing of the cDNAs induced by aluminium treatment and Pi starvation in cultured tobacco cell Physiol. Plant. 93 11–18
R. Galland B. Randoux J. Vasseur J.L. Hilbert (2001) ArticleTitleA glutathione-S-transferase cDNA identified by mRNA differential display is upregulated during somatic embryogenesis in Cichorium Biochim. Biophys. Acta 1522 212–216
H. Gong E.C. Pua (2004) ArticleTitleIdentification and expression of genes associated with shoot regeneration from leaf disc explants of mustard (Brassica juncea) in vitro Plant Sci. 167 1191–1201
M. Gonneau R. Mornet M. Laloue (1998) ArticleTitleA Nicotiana plumbaginifolia protein labeled with an azido cytokinin agonist is a glutathione S-transferase Physiol. Plant. 103 114–124
N. Holmberg L. Bülow (1998) ArticleTitleImproving stress tolerance in plants by gene transfer Trends Plant Sci. 3 61–66
M. Ikeda-Iwai M. Umehara S. Satoh H. Kamada (2003) ArticleTitleStress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana Plant J. 34 107–114
S. Immonen H. Anttila (1999) ArticleTitleCold treatment to enhance green plant regeneration from rye anther culture Plant Cell Tissue Organ Cult. 57 121–127
S. Immonen J. Robinson (2000) ArticleTitleStress treatments and ficoll for improving green plant regeneration in triticale anther culture Plant Sci. 150 77–84
D. Inzé M. Montagu Particlevan (1995) ArticleTitleOxidative stress in plants Curr. Opin. Biotechnol 6 153–158
H. Itzhaki W.R. Woodson (1993) ArticleTitleCharacterization of an ethylene-responsive glutathione S-transferase gene cluster in carnation Plant Mol. Biol. 22 43–58
E. Kitamiya S. Suzuki T. Sano T. Nagata (2000) ArticleTitleIsolation of two genes that were induced upon the initiation of somatic embryogenesis on carrot hypocotyls by high concentrations of 2,4-D Plant Cell Rep. 19 551–557
T. Kiyosue K. Yamaguchi-Shinozaki K. Shinozaki (1993) ArticleTitleCharacterization of two cDNAs (ERD11 and ERD13) for dehydration-inducible genes that encode putative glutathione S-transferase in Arabidopsis thaliana L FEBS Lett. 335 189–192
R. Kumria V.G. Sunnichan D.K. Das S.K. Gupta V.S. Reddy R.K. Bhatnagar S. Leelavathi (2003) ArticleTitleHigh-frequency somatic embryo production and maturation into normal plants in cotton (Gossypium hirsutum) through metabolic stress Plant Cell Rep. 21 635–639
A. Levine R. Tenhaken R. Dixon C. Lamb (1994) ArticleTitleH2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response Cell 79 583–593 Occurrence Handle10.1016/0092-8674(94)90544-4 Occurrence Handle1:CAS:528:DyaK2MXit1Glu7Y%3D Occurrence Handle7954825
J.P. Luo T.J. Jiang L.J. Pan (2001) ArticleTitleEnhanced somatic embryogenesis by salicylic acid of Astragalus adsurgensPall: relationship with H2O2 production and H2O2-metabolizing enzyme activities Plant Sci. 161 125–132
L. Loyall K. Uchida S. Braun M. Furuya H. Frohnmeyer (2000) ArticleTitleGlutathione and a UV light-induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures Plant Cell 12 1939–1950
H.G. Mang E.O. Kang J.H. Shim S. Kim K.Y. Park Y.S. Kim Y.Y. Bahk W.T. Kim (2004) ArticleTitleA proteomic analysis identifies glutathione S-transferase isoforms whose abundance is differentially regulated by ethylene during the formation of early root epidermis in Arabidopsis seedlings Biochem. Biophys. Acta 1676 231–239
K.A. Marrs (1996) ArticleTitleThe functions and regulation of glutathione-S-transferases in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 127–158
K.A. Marrs M.R. Alfenito A.M. Lloyd V. Walbot (1995) ArticleTitleA glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2 Nature 375 397–400 Occurrence Handle10.1038/375397a0 Occurrence Handle1:CAS:528:DyaK2MXmtVehsbs%3D Occurrence Handle7760932
R. Mundhara A. Rashid (2001) ArticleTitleRegeneration of shoot-buds on hypocotyls of Linum seedlings: a stress-related response Plant Sci. 161 19–25
T. Murashige F. Skoog (1962) ArticleTitleA revised medium for rapid growth and bioassays with tobacco tissue cultures Physiol. Plant. 15 473–497
D.J. Ockendon R. McClenaghan (1993) ArticleTitleEffect of silver nitrate and 2,4-D on anther culture of Brussels sprouts (Brassica oleracea var. gemmifera) Plant Cell Tissue Organ Cult. 32 41–46
K. Ogawa Y. Tasaka M. Mino Y. Tanaka M. Iwabuchi (2001) ArticleTitleAssociation of glutathione with flowering in Arabidopsis thaliana Plant Cell Physiol. 42 524–530
A.K. Papadakis K.A. Roubelakis-Angelakis (2002) ArticleTitleOxidative stress could be responsible for the recalcitrance of plant protoplasts Plant Physiol. Biochem. 40 549–559
A.N. Polidoros J.G. Scandalios (1999) ArticleTitleRole of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant. 106 112–120
E.C. Pua (1999) Morphogenesis in cell and tissue cultures: role of ethylene and polyamines W.Y. Soh S.S. Bhojeani (Eds) Morphogenesis in Plant Tissue Cultures. Kluwer Academic Publishers Dordrecht 255–303
E.C. Pua G.L. Chi (1993) ArticleTitleDe novo shoot morphogenesis and plant growth of mustard (Brassica juncea) in vitro in relation to ethylene Physiol. Plant. 88 467–474
E.C. Pua H. Gong (2004) Regulation of plant morphogenesis in vitro E.C. Pua C.J. Douglas (Eds) Biotechnology in Agriculture and Forestry Vol. 54: Brassica Springer-Verlag Berlin Heidelberg 83–102
E.C. Pua J.E.E. Lee (1995) ArticleTitleEnhanced de novoshoot morphogenesis in vitro by expression of antisense 1-aminocyclopropane-1-carboxylate oxidase gene in transgenic mustard plants Planta 196 69–76
M.V. Rao G. Paliyath D.P. Ormrod D.P. Murr C.B. Watkins (1997) ArticleTitleInfluence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes Plant Physiol. 115 137–149
J.P.H. Reade L.J. Milner A.H. Cobb (2004) ArticleTitleA role for glutathione S-transferases in resistance to herbicides in grasses Weed Sci. 52 468–474
P. Reymond H. Weber M. Damond E.E. Farmer (2000) ArticleTitleDifferential gene expression in response to mechanical wounding and insect feeding in Arabidopsis Plant Cell 12 707–719 Occurrence Handle10.1105/tpc.12.5.707 Occurrence Handle1:CAS:528:DC%2BD3cXjvFyhurk%3D Occurrence Handle10810145
J.P. Roustan A. Latché J. Falot (1989) ArticleTitleStimulation of Daucus carota somatic embryogenesis by inhibitors of ethylene synthesis: Cobalt and nickel Plant Cell Rep. 8 182–185
V.P. Roxas R.K. Smith E.R. Allen R.D. Allen (1997) ArticleTitleOverexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress Nat. Biotechnol. 15 988–991
M. Ruffer B. Steipe M.H. Zenk (1995) ArticleTitleEvidence against specific binding of salicylic acid to plant catalase FEBS Lett. 377 175–180
T.H. Rushmore C.B. Pickett (1993) ArticleTitleGlutathione S-transferases, structure, regulation, and therapeutic implications J Biol. Chem. 268 11475–11478
M.M. Seppänen T. Cardi M.B. Hyökki E. Pehu (2000) ArticleTitleCharacterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids Plant Sci. 153 125–133
Y.K. Sharma K.R. Davis (1994) ArticleTitleOzone-induced expression of stress-related genes in Arabidopsis thaliana Plant Physiol. 105 1089–1098
Y. Takahashi T. Nagata (1992) ArticleTitleParB: an auxin-regulated gene encoding glutathione S-transferase Proc. Natl. Acad. Sci. USA 89 56–59
T. Takesawa M. Ito H. Kanzaki N. Kameya I. Nakamura (2002) ArticleTitleOver-expression of glutathione S-transferase in transgenic rice enhances germination and growth at low temperature Mol. Breeding 9 93–101
W. Tang L.C. Harris V. Outhavong R.J. Newton (2004) ArticleTitleAntioxidants enhance in vitro plant regeneration by inhibiting the accumulation of peroxidase in Virginia pine (Pinus virginiana Mill.). Plant Cell Rep 22 871–877
D.A.M. Kop Particlevan der M. Schuyer B. Scheres B.J. Zaal Particlevan der P.J.J. Hooykaas (1996) ArticleTitleIsolation and characterization of an auxin-inducible glutathione S-transferase gene of Arabidopsis thaliana Plant Mol. Biol. 30 839–844
P.L. Vrinten T. Nakamura K.J. Kasha (1999) ArticleTitleCharacterization of cDNAs expressed in the early stages of microspore embryogenesis in barley (Hordeum vulgare L.). Plant Mol Biol. 41 455–463
U. Wagner R. Edwards D.P. Dixon F. Mauch (2002) ArticleTitleProbing the diversity of the Arabidopsis glutathione S-transferase gene family Plant Mol. Biol. 49 515–532
F. Xu E.S. Lagudah S.P. Moose D.E. Riechers (2002) ArticleTitleTandemly duplicated safener-induced glutathione S-transferase genes from Triticum tauschii contribute to genome- and organ-specific expression in hexaploid wheat Plant Physiol. 130 362–373
R. Zettl J. Schell K. Palme (1994) ArticleTitlePhotoaffinity labeling of Arabidopsis thaliana plasma membrane vesicles by 5-azido-[7–3H]indole-3-acetic acid: identification of a glutathione S-transferase Proc. Natl. Acad. Sci. USA 91 689–693
J. Zhou P.B. Goldsbrough (1993) ArticleTitleAn Arabidopsis gene with homology to glutathione S-transferase is regulated by ethylene Plant Mol. Biol. 22 517–523
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gong, H., Jiao, Y., Hu, Ww. et al. Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Mol Biol 57, 53–66 (2005). https://doi.org/10.1007/s11103-004-4516-1
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-004-4516-1