Glutathione S-transferase and aluminum toxicity in maize
Geraldo M. A. Cançado A B , Vicente E. De RosaA Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, 13083-970, Campinas, SP, Brazil.
B Departamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas, 13083-970, Campinas, SP, Brazil.
C Centro de Toxinologia Aplicada, Instituto Butantan, 05503-900, São Paulo, SP, Brazil.
D Departamento de Físico-Química, Instituto de Química, Universidade Estadual de Campinas, 13083-970, Campinas, SP, Brazil.
E Corresponding author. Email: menossi@unicamp.br
Functional Plant Biology 32(11) 1045-1055 https://doi.org/10.1071/FP05158
Submitted: 28 June 2005 Accepted: 29 July 2005 Published: 28 October 2005
Abstract
Aluminum (Al) toxicity induces changes in the expression of several genes, some of which are involved in plant responses to oxidative stress. Using mRNA differential display, we identified a maize Al-inducible cDNA encoding a glutathione S-transferase (GST). The gene was named GST27.2 owing to its homology to the maize gene GST27, which is known to be induced by xenobiotics. GST27.2 is present in the maize genome as a single copy and analysis of its expression pattern revealed that the gene is expressed mainly in the root tip. Expression was up-regulated in response to various Al and Cd concentrations in both Al-tolerant and Al-sensitive maize lines. Consistent with its role in plants, phylogenetic analysis of theta-type GSTs revealed that GST27.2 belongs to a group of proteins that respond to different stresses. Finally, structural analysis of the polypeptide chain indicates that the two amino acids that differ between GST27.2 and GST27 (E102K and P123L) could be responsible for alterations in activity and / or specificity. Together, these results suggest that GST27.2 may play an important part in plant defenses against Al toxicity.
Keywords: Al tolerance, Al toxicity, GST27.2, oxidative stress, Zea mays.
Acknowledgments
This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grants 04 / 05131-7 and 03 / 09536-9), European Commission (project INCO II RDT ICA4-CT-2000-30017), and PADCT / CNPq (project 62.0472 / 98.7). MM received a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). GMAC received a fellowship from the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). VERJ, JHF and LGM were recipients of fellowships from FAPESP.
Alfenito MR,
Souer E,
Goodman CD,
Buell R,
Mol J,
Koes R, Walbot V
(1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. The Plant Cell 10, 1135–1149.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alscher RG,
Erturk N, Heath LS
(2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Altschul SF,
Gish W,
Miller W,
Myers EW, Lipman DJ
(1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Arakawa Y,
Masaoka Y,
Sakai J,
Higo H, Higo K
(2002) An alfalfa gene similar to glutathione S-transferase is induced in root by iron deficiency. Soil Science and Plant Nutrition 48, 111–116.
Ausubel, FA ,
Brent, B ,
Kingston, RE ,
Moore, DD ,
Seidman, JG ,
Smith, JA ,
and
Struhl, K (1995).
Bilang J,
Macdonald H,
King PJ, Sturm A
(1993) A soluble auxin-binding protein from Hyoscyamus muticus is a glutathione-S-transferase. Plant Physiology 102, 29–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Board PG,
Coggan M,
Wilce MCJ, Parker MW
(1995) Evidence for an essential serine residue in the active-site of the theta-class glutathione transferases. Biochemical Journal 311, 247–250.
| PubMed |
Boscolo PRS,
Menossi M, Jorge RA
(2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62, 181–189.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen WQ,
Chao G, Singh KB
(1996) The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. The Plant Journal 10, 955–966.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dean JD,
Goodwin PH, Hsiang T
(2003)
Colletotrichum gloeosporioides infection induces differential expression of glutathione S-transferase genes in Malva pusilla. Functional Plant Biology 30, 821–828.
Deleers M,
Servais JP, Wulfert E
(1986) Neurotoxic cations induce membrane rigidification and membrane-fusion at micromolar concentrations. Biochimica et Biophysica Acta 855, 271–276.
| PubMed |
Delisle G,
Champoux M, Houde M
(2001) Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant and Cell Physiology 42, 324–333.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delledonne M,
Xia YJ,
Dixon RA, Lamb C
(1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Devi SR,
Yamamoto Y, Matsumoto H
(2003) An intracellular mechanism of aluminum tolerance associated with high antioxidant status in cultured tobacco cells. Journal of Inorganic Biochemistry 97, 59–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dixit V,
Pandey V, Shyam R
(2001) Differential anti-oxidative response to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). Journal of Experimental Botany 52, 1101–1109.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Droog F
(1997) Plant glutathione S-transferases, a tale of theta and tau. Journal of Plant Growth Regulation 16, 95–107.
Drummond RD,
Guimaraes CT,
Felix J,
Ninamango-Cardenas FE,
Carneiro NP,
Paiva E, Menossi M
(2001) Prospecting sugarcane genes involved in aluminum tolerance. Genetics and Molecular Biology 24, 221–230.
| Crossref | GoogleScholarGoogle Scholar |
Dudler R,
Hertig C,
Rebmann G,
Bull J, Mauch F
(1991) A pathogen-induced wheat gene encodes a protein homologous to glutathione-S-transferases. Molecular Plant–Microbe Interactions 4, 14–18.
| PubMed |
Edwards R,
Dixon DP, Walbot V
(2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends in Plant Science 5, 193–198.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ezaki B,
Yamamoto Y, Matsumoto H
(1995) Cloning and sequencing of the cDNAs induced by aluminum treatment and P-i starvation in cultured tobacco cells. Physiologia Plantarum 93, 11–18.
| Crossref | GoogleScholarGoogle Scholar |
Ezaki B,
Gardner RC,
Ezaki Y, Matsumoto H
(2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and / or oxidative stress. Plant Physiology 122, 657–665.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ezaki B,
Katsuhara M,
Kawamura M, Matsumoto H
(2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiology 127, 918–927.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fiser A,
Do RKG, Sali A
(2000) Modeling of loops in protein structures. Protein Science 9, 1753–1773.
| PubMed |
Frohman MA,
Dush MK, Martin GR
(1988) Rapid production of full-length cDNAs from rare transcripts — amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences USA 85, 8998–9002.
Hossain MZ, Fujita M
(2002) Purification of a phi-type glutathione S-transferase from pumpkin flowers, and molecular cloning of its cDNA. Bioscience, Biotechnology, and Biochemistry 66, 2068–2076.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goetzberger C,
Andrews CJ,
Jepson I,
Eulitz M,
Sandermann H, Schroeder P
(2000) Nucleotide sequence of a cDNA encoding a glutathione S-transferase (Accession No. AF184059) from wheat with activity towards the herbicide fenoxaprop-ethyl (PGR 00-008). Plant Physiology 122, 292.
Grant JJ, Loake GJ
(2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology 124, 21–29.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gratão PL,
Polle A,
Lea PJ, Azevedo RA
(2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology 32, 481–494.
| Crossref | GoogleScholarGoogle Scholar |
Grove G,
Zarlengo RP,
Timmerman KP,
Li NQ,
Tam MF, Tu CPD
(1988) Characterization and heterospecific expression of cDNA clones of genes in the maize GSH S-transferase multigene family. Nucleic Acids Research 16, 425–438.
| PubMed |
Hoisington, D ,
Khairallah, M ,
and
González-De-León, D (1994).
Irzyk G, Fuerst EP
(1993) Purification and characterization of a glutathione-S-transferase from benoxacor-treated maize (Zea mays). Plant Physiology 102, 803–810.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Irzyk G,
Potter S,
Ward E, Fuerst EP
(1995) A cDNA clone encoding the 27-kilodalton subunits of glutathione-S-transferase-IV from Zea mays. Plant Physiology 107, 311–312.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jepson I,
Lay VJ,
Holt DC,
Bright SWJ, Greenland AJ
(1994) Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione-S-transferase isoform-I, isoform-II and isoform-IV. Plant Molecular Biology 26, 1855–1866.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ketterer B, Meyer DJ
(1989) Glutathione transferase — a possible role in the detoxication and repair of DNA and lipid hydroperoxides. Mutation Research 214, 33–40.
| PubMed |
Kiyosue T,
Yamaguchishinozaki K, Shinozaki K
(1993) Characterization of 2 cDNAs (Erd11 and Erd13) for dehydration-inducible genes that encode putative glutathione S-transferases in Arabidopsis thaliana. FEBS Letters 335, 189–192.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Klinedinst S,
Pascuzzi P,
Redman J,
Desai M, Arias J
(2000) A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Molecular Biology 42, 679–688.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kumar S,
Tamura K, Nei M
(1994) Mega — molecular evolutionary genetics analysis software for microcomputers. Computer Applications in the Biosciences 10, 189–191.
| PubMed |
Lamb C, Dixon RA
(1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lands LC,
Grey VL, Smountas AA
(1999) Effect of supplementation with a cysteine donor on muscular performance. Journal of Applied Physiology 87, 1381–1385.
| PubMed |
Laskowski RA,
McArthur MW,
Moss DS, Thornton JM
(1993) PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26, 283–291.
| Crossref | GoogleScholarGoogle Scholar |
Lindahl E,
Hess B, Van Der Spoel D
(2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis. Journal of Molecular Modeling (Online) 7, 306–317.
Logemann J,
Schell J, Willmitzer L
(1987) Improved method for the isolation of RNA from plant-tissues. Analytical Biochemistry 163, 16–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mannervik B, Danielson UH
(1988) Glutathione transferases — structure and catalytic activity. Critical Reviews in Biochemistry and Molecular Biology 23, 283–337.
Marrs KA
(1996) The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 127–158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marrs KA, 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mauch F, Dudler R
(1993) Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiology 102, 1193–1201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McGonigle B,
Keeler SJ,
Lan SMC,
Koeppe MK, O’Keefe DP
(2000) A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiology 124, 1105–1120.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moon DH,
Ottoboni LMM,
Souza AP,
Sibov ST,
Gaspar M, Arruda P
(1997) Somaclonal-variation-induced aluminum-sensitive mutant from an aluminum-inbred maize tolerant line. Plant Cell Reports 16, 686–691.
| Crossref | GoogleScholarGoogle Scholar |
Neuefeind T,
Huber R,
Reinemer P,
Knablein J,
Prade L,
Mann K, Bieseler B
(1997a) Cloning, sequencing, crystallization and x-ray structure of glutathione S-transferase-III from Zea mays var. mutin: a leading enzyme in detoxification of maize herbicides. Journal of Molecular Biology 274, 577–587.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neuefeind T,
Huber R,
Dasenbrock H,
Prade L, Bieseler B
(1997b) Crystal structure of herbicide-detoxifying maize glutathione S-transferase-I in complex with lactoylglutathione: evidence for an induced-fit mechanism. Journal of Molecular Biology 274, 446–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pan JW,
Zhu MY, Chen H
(2001) Aluminum-induced cell death in root-tip cells of barley. Environmental and Experimental Botany 46, 71–79.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Potikha TS,
Collins CC,
Johnson DI,
Delmer DP, Levine A
(1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiology 119, 849–858.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Prade L,
Huber R, Bieseler B
(1998) Structures of herbicides in complex with their detoxifying enzyme glutathione S-transferase — explanations for the selectivity of the enzyme in plants. Structure 6, 1445–1452.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reinemer P,
Prade L,
Hof P,
Neuefeind T, Huber R , et al.
(1996) Three-dimensional structure of glutathione S-transferase from Arabidopsis thaliana at 2.2 angstrom resolution: structural characterization of herbicide-conjugating plant glutathione S-transferases and a novel active site architecture. Journal of Molecular Biology 255, 289–309.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Richards KD,
Schott EJ,
Sharma YK,
Davis KR, Gardner RC
(1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology 116, 409–418.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saitou N, Nei M
(1987) The neighbor-joining method — a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
| PubMed |
Sali A, Blundell TL
(1993) Comparative protein modeling by satisfaction of spatial restraints. Journal of Molecular Biology 234, 779–815.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sambrook, J ,
Fristch, EF ,
and
Maniatis, T (1989).
Sandermann H
(1994) Higher-plant metabolism of xenobiotics — the green liver concept. Pharmacogenetics 4, 225–241.
| PubMed |
Scalla R, Roulet A
(2002) Cloning and characterization of a glutathione S-transferase induced by a herbicide safener in barley (Hordeum vulgare). Physiologia Plantarum 116, 336–344.
| Crossref | GoogleScholarGoogle Scholar |
Shah DM,
Hironaka CM,
Wiegand RC,
Harding EI,
Krivi GG, Tiemeier DC
(1986) Structural-analysis of a maize gene coding for glutathione-S-transferase involved in herbicide detoxification. Plant Molecular Biology 6, 203–211.
| Crossref | GoogleScholarGoogle Scholar |
Snowden KC, Gardner RC
(1993) Genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiology 103, 855–861.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soranzo N,
Gorla MS,
Mizzi L,
De Toma G, Frova C
(2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Molecular Genetics and Genomics 271, 511–521.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Takahashi Y, Nagata T
(1992) Parb — an auxin-regulated gene encoding glutathione-S-transferase. Proceedings of the National Academy of Sciences USA 89, 56–59.
Theodoulou FL,
Clark IM,
He XL,
Pallett KE,
Cole DJ, Hallahan DL
(2003) Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Management Science 59, 202–214.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thompson JD,
Gibson TJ,
Plewniak F,
Jeanmougin F, Higgins DG
(1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van Aalten DMF,
Bywater R,
Findlay JBC,
Hendlich M,
Hooft RWW, Vriend G
(1996) PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. Journal of Computer-Aided Molecular Design 10, 255–262.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Widersten M,
Bjornestedt R, Mannervik B
(1996) Involvement of the carboxyl groups of glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry 35, 7731–7742.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wilce MCJ, Parker MW
(1994) Structure and function of glutathione S-transferases. Biochimica et Biophysica Acta 1205, 1–18.
| PubMed |
Yamamoto Y,
Kobayashi Y,
Devi SR,
Rikiishi S, Matsumoto H
(2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiology 128, 63–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |