Skip to main content
Log in

Organisation and structural evolution of the rice glutathione S-transferase gene family

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Glutathione S-transferases (GSTs) comprise a large family of key defence enzymes against xenobiotic toxicity. Here we describe the comprehensive characterisation of this important multigene family in the model monocot species rice [Oryza sativa (L.)]. Furthermore, we investigate the molecular evolution of the family based on the analysis of (1) the patterns of within-genome duplication, and (2) the phylogenetic relationships and evolutionary divergence among rice, Arabidopsis, maize and soybean GSTs. By in-silico screening of the EST and genome divisions of the Genbank/EMBL/DDBJ database we have isolated 59 putative genes and two pseudogenes, making this the largest plant GST family characterised to date. Of these, 38 (62%) are represented by genomic and EST sequences and 23 (38%) are known only from their genomic sequences. A preliminary survey of EST collections shows a large degree of variability in gene expression between different tissues and environmental conditions, with a small number of genes (13) accounting for 80% of all ESTs. Rice GSTs are organised in four main phylogenetic classes, with 91% of all rice genes belonging to the two plant-specific classes Tau (40 genes) and Phi (16 genes). Pairwise identity scores range between 17 and 98% for proteins of the same class, and 7 and 21% for interclass comparisons. Rapid evolution by gene duplication is suggested by the discovery of two large clusters of 7 and 23 closely related genes on chromosomes 1 and 10, respectively. A comparison of the complete GST families in two monocot and two dicot species suggests a monophyletic origin for all Theta and Zeta GSTs, and no more than three common ancestors for all Phi and Tau genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alfenito MR, Souer E, Godman CD, Buell R, Mol J, Koes R, Walbot V (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10:1135–1149

    Google Scholar 

  • Altschul SF, Lipman DJ (1990) Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87:5509–5513

    CAS  PubMed  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–219

    CAS  Google Scholar 

  • Bartling D, Radzio R, Steiner U, Weiler EW (1993) A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Eur J Biochem 216:579–586

    CAS  PubMed  Google Scholar 

  • Bilang J, Sturm A (1995) Cloning and characterization of a glutathione S-transferase that can be photolabeled with 5-azido-indole-3-acetic acid. Plant Physiol 109:253–260

    Article  CAS  PubMed  Google Scholar 

  • Board PG, Baker RT, Chelvanayagam G, Jermiin LS (1997) Zeta, a novel class of glutathione transferases in a large range of species from plants to humans. Biochem J 328:929–935

    CAS  PubMed  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Chen M (2002) An integrated physical and genetic map of the rice genome. IRGSP Meeting Report 2002 (available at http://demeter.bio.bnl.gov/Tsukuba02.html)

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    Article  CAS  PubMed  Google Scholar 

  • Davenport RJ (2001) Syngenta finishes, consortium goes on. Science 291:807a

    Article  Google Scholar 

  • Devos KM, Beales J, Nagamura Y, Sasaki T (1999) Arabidopsis-rice: will colinearity allow prediction across the eudicot-monocot divide? Genome Res 9:825–829

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266

    CAS  Google Scholar 

  • Dixon DP, Cole DJ, Edwards R (2000) Characterisation of a zeta class glutathione transferase form Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch Biochem Biophys 384:407–412

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1–3004.10

    Article  Google Scholar 

  • Droog F (1997) Plant glutathione S-transferases, a tale of Theta and Tau. J Plant Growth Regul 16:95–107

    CAS  Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    CAS  PubMed  Google Scholar 

  • Feng Q, et al (2002) Sequence analysis of rice chromosome 4. Nature 420:316–320

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Cañon JM, Peñalva MA (1998) Characterization of a fungal maleylacetoacetate isomerase gene and identification of its human homologue. J Biol Chem 273:328–337

    Google Scholar 

  • Fuerst EP, Gronwald JW (1986) Induction of rapid mechanism of metolachlor in sorghum ( Sorgum bicolor) shoots by CGA-92194 and other antidotes. Weed Sci 34:354–361

    CAS  Google Scholar 

  • Goff SA, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. japonica). Science 296:92–100

    CAS  PubMed  Google Scholar 

  • Harushima Y, et al (1998) A high-density rice linkage map with 2275 markers using a single F2 population. Genetics 148:479–494

    CAS  PubMed  Google Scholar 

  • Hatton PJ, Cummins I, Cole DJ, Edwards R (1999) Glutathione transferases involved in herbicide detoxification in the leaves of Setaria faberi (giant foxtail). Physiol Plantarum 105:9–16

    Article  CAS  Google Scholar 

  • Hayes JD, Pulford DJ (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isozymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600

    CAS  PubMed  Google Scholar 

  • Henikoff S, Henikoff JG (1994) Protein family classification based on searching a database of blocks. Genomics 19:97–107

    CAS  PubMed  Google Scholar 

  • Kampranis SC, Damianova R, Atallah M, Toby G, Kondi G, Tsichlis PN, Makris AM (2000) A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. J Biol Chem 275(38): 29207–29216

    CAS  PubMed  Google Scholar 

  • Loyall L, Uchida K, Brown S, Furuya M, Frohnmeyer H (2000) Glutathione and a UV-light induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 12:1939–1950

    Article  CAS  PubMed  Google Scholar 

  • Marrs KA (1996) The functions and regulation of plant glutathione S-transferases. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    CAS  Google Scholar 

  • Mayer K, et al (2001) Conservation of microstructure between a sequenced region of the genome of rice and multiple segments of the genome of Arabidopsis thaliana. Genome Res 11:1167–1174

    CAS  PubMed  Google Scholar 

  • McGonigle B, Keeler SJ, Lau S-MC, 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 Physiol 124:1105–1120

    CAS  PubMed  Google Scholar 

  • Mueller LA, Godman CD, Silady RA, Walbot V (2000) AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid binding protein. Plant Physiol 123:1561–1570

    PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Berlin-Heidelberg-New York

  • Ohta T (2000) Evolution of gene families. Gene 259:45–52

    Article  CAS  PubMed  Google Scholar 

  • Pickett CB, Lu AY (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem 58:743–764

    Article  CAS  PubMed  Google Scholar 

  • Rossini L, Jepson I, Greenland A, Sari-Gorla M (1996) Characterisation of GST isoforms in three maize inbred lines exhibiting differential sensitivity to alachlor. Plant Physiol 112:1595–1600

    CAS  PubMed  Google Scholar 

  • Rossini L, Frova C, Pè ME, Mizzi L, Sari Gorla M (1998) Alachlor regulation of maize glutathione S-transferase genes. Pestic Biochem Physiol 60:205–211

    Article  CAS  Google Scholar 

  • Saji S, Umehara Y, Antonio BA, Yamane H, Tanoue H, Baba T, Aoki H, Ishige N, Wu J, Koike K, Matsumoto T, Sasaki T (2001) A physical map with yeast artificial chromosome (YAC) clones covering 63% of the 12 rice chromosomes. Genome 44:32–37

    Article  PubMed  Google Scholar 

  • Sakata K, Nagasaki H, Idonuma A, Waki K, Kise M, Sasaki T (1999) A computer program for prediction of gene domain on rice genome sequence. The 2nd Georgia Tech International Conference on Bioinformatics, Abstracts p 78

  • Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K (2002) RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102

    Article  CAS  PubMed  Google Scholar 

  • Salse J, Piegu B, Cooke R, Delseny M (2002) Synteny between Arabidopsis thaliana and rice at the genome level: a tool to identify conservation in the ongoing genome sequencing project. Nucleic Acid Res 30:2316–2328

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Burr B (2000) International Rice Genome Sequencing Project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–141

    CAS  PubMed  Google Scholar 

  • Sasaki T, et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316

    Article  CAS  PubMed  Google Scholar 

  • The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity and evolution of rice chromosome 10. Science 300:1566–1569

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Wagner A (2001) Birth and death of duplicated genes in completely sequenced eukaryotes. Trends Genet 17:237–239

    CAS  PubMed  Google Scholar 

  • Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532

    Article  CAS  PubMed  Google Scholar 

  • Ware D, Jaiswal P, Ni J, Pan X, Chang K, Clark K, Taytelman L, Schmidt S, Zhao W, Cartinhour S, McCouch S, Stein L (2002) Gramene: a resource for comparative grass genomics. Nucleic Acid Res 30:103–105

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989) Date of monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    CAS  PubMed  Google Scholar 

  • Wu J, Cramer CL, Hatzios KK (1999) Characterization of two cDNAs encoding glutathione S-transferases in rice and induction of their transcripts by the herbicide safener fenchlorim. Physiol Plantarum 105:102–108

    Article  CAS  Google Scholar 

  • Wu J, et al (2002) A comprehensive rice transcript map containing 6591 EST sites. Plant Cell 14:525–535

    CAS  PubMed  Google Scholar 

  • Yu J, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. indica). Science 296:79–92

    CAS  PubMed  Google Scholar 

  • Yuan Q, Hill J, Hsiao J, Moffat K, Ouyang S, Cheng Z, Jiang J, Buell CR (2002) Genome sequencing of a 239-kb region of rice chromosome 10L reveals a high frequency of gene duplication an a large chloroplast DNA insertion. Mol Genet Genomics 267:713–720

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank Roberta Rizzardi and Ester Baldrighi who participated to the initial stages of this work, and two anonymous referees for useful comments on a previous version of the manuscript. The cDNA clones were received from the MAFF DNA Bank (Tsukuba, Japan). This work was supported by grants from the Italian Ministry of Education and Research (MIUR PRIN1999, MIUR PRIN2002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Frova.

Additional information

Communicated by M.-A. Grandbastien

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soranzo, N., Sari Gorla, M., Mizzi, L. et al. Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271, 511–521 (2004). https://doi.org/10.1007/s00438-004-1006-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-004-1006-8

Keywords

Navigation