Molecular Genetics and Genomics

, Volume 271, Issue 5, pp 511–521 | Cite as

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

  • N. Soranzo
  • M. Sari Gorla
  • L. Mizzi
  • G. De Toma
  • C. Frova
Original Paper

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.

Keywords

Glutathione S-transferases Gene families Genomic organization Evolution 

Notes

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).

Supplementary material

supp.pdf (147 kb)
(PDF 147 KB)

References

  1. 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 10:1135–1149Google Scholar
  2. Altschul SF, Lipman DJ (1990) Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87:5509–5513PubMedGoogle Scholar
  3. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–219Google Scholar
  4. Bartling D, Radzio R, Steiner U, Weiler EW (1993) A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Eur J Biochem 216:579–586PubMedGoogle Scholar
  5. 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 109:253–260CrossRefPubMedGoogle Scholar
  6. 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 328:929–935PubMedGoogle Scholar
  7. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94CrossRefPubMedGoogle Scholar
  8. 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)
  9. 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 18:285–292CrossRefPubMedGoogle Scholar
  10. Davenport RJ (2001) Syngenta finishes, consortium goes on. Science 291:807aCrossRefGoogle Scholar
  11. Devos KM, Beales J, Nagamura Y, Sasaki T (1999) Arabidopsis-rice: will colinearity allow prediction across the eudicot-monocot divide? Genome Res 9:825–829CrossRefPubMedGoogle Scholar
  12. Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266Google Scholar
  13. 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 384:407–412CrossRefPubMedGoogle Scholar
  14. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1–3004.10CrossRefGoogle Scholar
  15. Droog F (1997) Plant glutathione S-transferases, a tale of Theta and Tau. J Plant Growth Regul 16:95–107Google Scholar
  16. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198PubMedGoogle Scholar
  17. Feng Q, et al (2002) Sequence analysis of rice chromosome 4. Nature 420:316–320CrossRefPubMedGoogle Scholar
  18. Fernandez-Cañon JM, Peñalva MA (1998) Characterization of a fungal maleylacetoacetate isomerase gene and identification of its human homologue. J Biol Chem 273:328–337Google Scholar
  19. Fuerst EP, Gronwald JW (1986) Induction of rapid mechanism of metolachlor in sorghum ( Sorgum bicolor) shoots by CGA-92194 and other antidotes. Weed Sci 34:354–361Google Scholar
  20. Goff SA, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. japonica). Science 296:92–100PubMedGoogle Scholar
  21. Harushima Y, et al (1998) A high-density rice linkage map with 2275 markers using a single F2 population. Genetics 148:479–494PubMedGoogle Scholar
  22. 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 105:9–16CrossRefGoogle Scholar
  23. 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 30:445–600PubMedGoogle Scholar
  24. Henikoff S, Henikoff JG (1994) Protein family classification based on searching a database of blocks. Genomics 19:97–107PubMedGoogle Scholar
  25. 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): 29207–29216PubMedGoogle Scholar
  26. 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 12:1939–1950CrossRefPubMedGoogle Scholar
  27. Marrs KA (1996) The functions and regulation of plant glutathione S-transferases. Annu Rev Plant Physiol Plant Mol Biol 47:127–158Google Scholar
  28. 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 11:1167–1174PubMedGoogle Scholar
  29. 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 124:1105–1120PubMedGoogle Scholar
  30. 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 123:1561–1570PubMedGoogle Scholar
  31. Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Berlin-Heidelberg-New YorkGoogle Scholar
  32. Ohta T (2000) Evolution of gene families. Gene 259:45–52CrossRefPubMedGoogle Scholar
  33. Pickett CB, Lu AY (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem 58:743–764CrossRefPubMedGoogle Scholar
  34. 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 112:1595–1600PubMedGoogle Scholar
  35. Rossini L, Frova C, Pè ME, Mizzi L, Sari Gorla M (1998) Alachlor regulation of maize glutathione S-transferase genes. Pestic Biochem Physiol 60:205–211CrossRefGoogle Scholar
  36. 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 44:32–37CrossRefPubMedGoogle Scholar
  37. 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 78Google Scholar
  38. 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 30:98–102CrossRefPubMedGoogle Scholar
  39. 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 30:2316–2328CrossRefPubMedGoogle Scholar
  40. Sasaki T, Burr B (2000) International Rice Genome Sequencing Project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–141PubMedGoogle Scholar
  41. Sasaki T, et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316CrossRefPubMedGoogle Scholar
  42. The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity and evolution of rice chromosome 10. Science 300:1566–1569CrossRefPubMedGoogle Scholar
  43. 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 22:4673–4680PubMedGoogle Scholar
  44. Wagner A (2001) Birth and death of duplicated genes in completely sequenced eukaryotes. Trends Genet 17:237–239PubMedGoogle Scholar
  45. Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532CrossRefPubMedGoogle Scholar
  46. 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 30:103–105CrossRefPubMedGoogle Scholar
  47. 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 86:6201–6205PubMedGoogle Scholar
  48. 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 105:102–108CrossRefGoogle Scholar
  49. Wu J, et al (2002) A comprehensive rice transcript map containing 6591 EST sites. Plant Cell 14:525–535PubMedGoogle Scholar
  50. Yu J, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. indica). Science 296:79–92PubMedGoogle Scholar
  51. 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 267:713–720CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • N. Soranzo
    • 1
    • 2
  • M. Sari Gorla
    • 1
  • L. Mizzi
    • 1
  • G. De Toma
    • 1
  • C. Frova
    • 1
  1. 1.Department of Biomolecular Sciences and BiotechnologyUniversity of MilanMilanoItaly
  2. 2.Department of BiologyUniversity College LondonLondonUK

Personalised recommendations