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.
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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
Altschul SF, Lipman DJ (1990) Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87:5509–5513
Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–219
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
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
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
Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94
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
Davenport RJ (2001) Syngenta finishes, consortium goes on. Science 291:807a
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
Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266
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
Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1–3004.10
Droog F (1997) Plant glutathione S-transferases, a tale of Theta and Tau. J Plant Growth Regul 16:95–107
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
Feng Q, et al (2002) Sequence analysis of rice chromosome 4. Nature 420:316–320
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
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
Goff SA, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. japonica). Science 296:92–100
Harushima Y, et al (1998) A high-density rice linkage map with 2275 markers using a single F2 population. Genetics 148:479–494
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
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
Henikoff S, Henikoff JG (1994) Protein family classification based on searching a database of blocks. Genomics 19:97–107
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
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
Marrs KA (1996) The functions and regulation of plant glutathione S-transferases. Annu Rev Plant Physiol Plant Mol Biol 47:127–158
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
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
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
Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Berlin-Heidelberg-New York
Ohta T (2000) Evolution of gene families. Gene 259:45–52
Pickett CB, Lu AY (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem 58:743–764
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
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
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
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
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
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
Sasaki T, et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316
The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity and evolution of rice chromosome 10. Science 300:1566–1569
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
Wagner A (2001) Birth and death of duplicated genes in completely sequenced eukaryotes. Trends Genet 17:237–239
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
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
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
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
Wu J, et al (2002) A comprehensive rice transcript map containing 6591 EST sites. Plant Cell 14:525–535
Yu J, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp. indica). Science 296:79–92
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
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).
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Communicated by M.-A. Grandbastien
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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
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DOI: https://doi.org/10.1007/s00438-004-1006-8