Plant Molecular Biology

, Volume 55, Issue 3, pp 343–367

Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1

  • Zhiwei Xu
  • Luis Escamilla-Treviño
  • Lihui Zeng
  • Mallikarjun Lalgondar
  • David Bevan
  • Brenda Winkel
  • Ali Mohamed
  • Chi-Lien Cheng
  • Ming-Che Shih
  • Jonathan Poulton
  • Asim Esen
Article

Abstract

In plants, Glycoside Hydrolase (GH) Family 1 β-glycosidases are believed to play important roles in many diverse processes including chemical defense against herbivory, lignification, hydrolysis of cell wall-derived oligosaccharides during germination, and control of active phytohormone levels. Completion of the Arabidopsis thalianagenome sequencing project has enabled us, for the first time, to determine the total number of Family 1 members in a higher plant. Reiterative database searches revealed a multigene family of 48 members that includes eight probable pseudogenes. Manual reannotation and analysis of the entire family were undertaken to rectify existing misannotations and identify phylogenetic relationships among family members. Forty-seven members (designated BGLU1 through BGLU47) share a common evolutionary origin and were subdivided into approximately 10 subfamilies based on phylogenetic analysis and consideration of intron–exon organizations. The forty-eighth member of this family (At3g06510; sfr2) is a β-glucosidase-like gene that belongs to a distinct lineage. Information pertaining to expression patterns and potential functions of Arabidopsis GH Family 1 members is presented. To determine the biological function of all family members, we intend to investigate the substrate specificity of each mature hydrolase after its heterologous expression in the Pichia pastoris expression system. To test the validity of this approach, the BGLU44-encoded hydrolase was expressed in P. pastoris and purified to homogeneity. When tested against a wide range of natural and synthetic substrates, this enzyme showed a preference for β-mannosides including 1,4-β-D-mannooligosaccharides, suggesting that it may be involved in A. thaliana in degradation of mannans, galactomannans, or glucogalactomannans. Supporting this notion, BGLU44 shared high sequence identity and similar gene organization with tomato endosperm β-mannosidase and barley seed β-glucosidase/β-mannosidase BGQ60.

Arabidopsis β-mannosidase functional genomics Glycoside Hydrolase Family 1 heterologous expression Pichia 

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References

  1. Agerbirk, N., Petersen, B. L., Olsen, C. E., Halkier, B. A. and Nielsen, J. K. 2001. 1, 4-Dimethoxyglucobrassicin in Barbarea and 4-hydroxyglucobrassicin in Arabidopsis and Brassica. J. Agric. Food Chem. 49: 1502-1507.PubMedGoogle Scholar
  2. Altschul, F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.PubMedGoogle Scholar
  3. Andréasson, E., Jørgensen, L. B., Höglund, A.-S., Rask, L. and Meijer, J. 2001. Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiol. 127: 1750-1763.PubMedGoogle Scholar
  4. Bailey, R. W. and Bourne, E. J. 1960. Color reagents given by sugars and diphenylamine-aniline spray reagents on paper chromatograms. J. Chromatogr. 4: 206-213.Google Scholar
  5. Babcock, G. D. and Esen, A. 1994. Substrate specificity of maize b-glucosidase. Plant Sci. 101: 31-39.Google Scholar
  6. Barrett, T., Suresh, C. G., Tolley, S. P., Dodson, E. J. and Hughes, M. A. 1995. The crystal structure of a cyanogenic bglucosidase from white sweet clover, a family 1 glycosyl hydrolase. Structure 3: 951-960.PubMedGoogle Scholar
  7. Béguin, P. 1990. Molecular biology of cellulose degradation. Annu. Rev. Microbiol 44: 219-248.PubMedGoogle Scholar
  8. Berrin, J. G., Czjzek, M., Kroon, P. A., McLauchlan, W. R., Puigserver, A., Williamson, G. and Juge, N. 2003. Substrate (aglycone) specificity of human cytosolic beta-glucosidase. Biochem. J. 373: 41-48.PubMedGoogle Scholar
  9. Blanc, G., Hokamp, K. and Wolfe, K. H. 2003. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137-144.PubMedGoogle Scholar
  10. Bloor, S. J. and Abrahams, S. 2002. The structure of the major anthocyanin in Arabidopsis thaliana. Phytochemistry 59: 343-346.PubMedGoogle Scholar
  11. Brown, J. W. S. and Simpson, C. G. 1998. Splice site selection in plant pre-mRNA splicing. Annu. Rev. Plant Physiol. Mol. Biol. 49: 77-95.Google Scholar
  12. Burmeister, W. P., Cottaz, S., Driguez, H., Iori, R., Palmieri, S. and Henrissat, B. 1997. The crystal structure of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and activesite machinery of an S-glycosidase. Structure 5: 663-675.PubMedGoogle Scholar
  13. Burset, M., Seledtsov, I. A. and Solovyev, V. V. 2000. Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res. 28: 4364-4375.PubMedGoogle Scholar
  14. Callard, D., Axelos, M. and Mazzolini, L. 1996. Novel molecular markers for late phases of the growth cycle of Arabidopsis thaliana cell-suspension cultures are expressed during organ senescence. Plant Physiol. 112: 705-715.PubMedGoogle Scholar
  15. Chivasa, S., Ndimba, B. K., Simon, W. J., Robertson, D., Yu, X.-L., Knox, J. P., Bolwell, P. and Slabas, A. R. 2002. Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 23: 1754-1765.PubMedGoogle Scholar
  16. Conn, E. E. 1993. b-Glycosidases in plants. Substrate specificity. In: A. Esen (Ed. ) b-Glucosidases: Biochemistry and Molecular Biology, ACS Symposium Series 533. American Chemical Society, Washington, DC, pp. 15-26.Google Scholar
  17. Coutinho, P. M. and Henrissat, B. 1999. Carbohydrate-Active Enzymes server at URL: http://afmb. cnrs-mrs. fr/_cazy/ CAZY/index. html.Google Scholar
  18. Cregg, J. M., Vedvick, T. S. and Raschke, W. C. 1993. Recent advances in the expression of foreign genes in Pichia pastoris. Biotechnology 11: 905-910.PubMedGoogle Scholar
  19. Czjzek, M., Cicek, M., Zamboni, V., Bevan, D. R., Henrissat, B. and Esen, A. 2000. The mechanism of substrate (aglycone) specificity in b-glucosidases is revealed by crystal structures of mutant maize b-glucosidase-DIMBOA,-DIMBOAGlc, and-dhurrin complexes. Proc. Natl. Acad. Sci. USA 97: 13555-13560.PubMedGoogle Scholar
  20. Dharmawardhana, D. P., Ellis, B. E. and Carlson, J. E. 1995. A b-glucosidase from lodgepole pine specific for the lignin precursor coniferin. Plant Physiol. 107: 331-339.PubMedGoogle Scholar
  21. Dharmawardhana, D. P., Ellis, B. E. and Carlson, J. E. 1999. cDNA cloning and heterologous expression of coniferin bglucosidase. Plant Mol. Biol. 40: 365-372.PubMedGoogle Scholar
  22. Esen, A. 1996. Zea mays beta-D-glucosidase (glu1) gene (GenBank Accession No. U44773). Direct submission.Google Scholar
  23. Esen, A. and Stetler, D. A. 1993. Subcellular localization of maize b-glucosidase.Maize Genet. Coop. News Lett. 67: 19-20.Google Scholar
  24. Falk, A. and Rask, L. 1995. Expression of a zeatin-O-glucosidedegrading b-glucosidase in Brassica napus. Plant Physiol. 108: 1369-1377.PubMedGoogle Scholar
  25. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.Google Scholar
  26. Fowler, T. 1993. Deletion of the Trichoderma reesei b-glucosidase gene, bgl1. In: A. Esen (Ed. ) b-Glucosidases: Biochemistry and Molecular Biology, ACS Symposium Series 533. American Chemical Society, Washington, DC, pp. 56-65.Google Scholar
  27. Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Hishida, I. and Watanabe, A. 2001. Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol. Plant. 111: 345-352.PubMedGoogle Scholar
  28. Gallardo, K., Job, C., Groot, S. P. C., Puype, M., Demol, H., Vanderkerckhove, J. and Job, D. 2001. Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol. 126: 835-848PubMedGoogle Scholar
  29. Gualberto, J. M., Schell, J. and Palme, K. 1998. Arabidopsis thaliana beta-glucosidase (GLUC) mRNA, complete cds (direct sequence submission to GenBank).Google Scholar
  30. Haas, B. J., Volfovsky, N., Town, C. D., Troukhan, M., Alexandrov, N., Feldmann, K. A., Flavell, R. B., White, O. and Salzberg, S. L. 2002. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol. 3: research 00291-002912.Google Scholar
  31. Handford, M. G., Baldwin, T. C., Goubet, F., Prime, T. A., Miles, J., Yu, X. and Dupree, P. 2003. Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta 218: 27-36.PubMedGoogle Scholar
  32. Hagemeier, J., Schneider, B., Oldham, N. J. and Hahlbrock, K. 2001. Accumulation of soluble and wall-bound indolic metabolites in Arabidopsis thaliana leaves infected with virulent and avirulent Pseudomonas syringae pathovar tomato strains. Proc. Natl. Acad. Sci. USA 98: 753-758.PubMedGoogle Scholar
  33. Hartel, F. V. and Brandt, A. 2002. Characterization of a Brassica napus myrosinase expressed and secreted by Pichia pastoris. Protein Expr Purif. 24: 221-226.PubMedGoogle Scholar
  34. Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280: 309-316.PubMedGoogle Scholar
  35. Henrissat, B. and Davies, G. J. 1997. Structural and sequencebased classification of glycosyl hydrolases. Curr. Opin. Struct. Biol. 7: 637-644.PubMedGoogle Scholar
  36. Higgins, D. R. and Cregg, J. M. 1999. Introduction to Pichia pastoris. In: D. R. Higgins and J. M. Cregg (Eds. ) Pichia Protocols, Methods in Molecular Biology 103, Humana Press, Towata, NJ, pp. 1-15.Google Scholar
  37. Hogge, L. R., Reed, D. W., Underhill, E. W. and Haughn, G. W. 1988. HPLC separation of glucosinolates from leaves and seeds of Arabidopsis thaliana and their identification using thermospray liquid chromatography-mass spectrometry. J. Chromatogr. Sci. 26: 551-556.Google Scholar
  38. Hösel, W. and Barz, W. 1975. b-Glucosidases from Cicer arietinum L. Purification and properties of isoflavone-7-Oglucoside-specific b-glucosidases. Eur. J. Biochem. 57: 607-616.PubMedGoogle Scholar
  39. Hösel, W. and Nahrstedt, A. 1975. Spezifische Glucosidasen fuer das Cyanoglucosid Triglochinin: Reinigung und Charakterisierung von b-Glucosidasen aus Alocasia macrorrhiza Schott. Hoppe-Seyler's Z. Physiol. Chem. 356: 1265-1275.Google Scholar
  40. Hösel, W. and Todenhagen, R. 1980. Characterization of a bglucosidase from Glycine max which hydrolyses coniferin and syringin. Phytochemistry 19: 331-339.Google Scholar
  41. Hösel, W., Tober, I., Eklund, S. H. and Conn, E. E. 1987. Characterization of b-glucosidases with high specificity for 365 the cyanogenic glucoside dhurrin in Sorghum bicolor (L. ) Moench seedlings. Arch. Biochem. Biophys. 252: 152-162.PubMedGoogle Scholar
  42. Initiative, A. G. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.PubMedGoogle Scholar
  43. Inoue, K. and Ebizuka, Y. 1996. Purification and characterization of a beta-glucosidase which converts furostanol glycosides to spirostanol glycosides from Costus speciosus. Adv. Exp. Med. Biol. 404: 57-69.PubMedGoogle Scholar
  44. Inoue, K., Shibuya, M., Yamamoto, K. and Ebizuka, Y. 1996. Molecular cloning and bacterial expression of a cDNA encoding furostanol glycoside 26-O-beta-glucosidase of Costus speciosus. FEBS Lett. 389: 273-277.PubMedGoogle Scholar
  45. Kosuge, T. and Conn, E. E. 1961. The metabolism of aromatic compounds in higher plants. III. The b-glucosides of o-coumaric, coumarinic, and melilotic acids. J. Biol. Chem. 236: 1617-1621.PubMedGoogle Scholar
  46. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.PubMedGoogle Scholar
  47. Leah, R., Kigel J., Svendsen, I. and Mundy, J. 1995. Biochemical and molecular characterization of a barley seed bglucosidase. J. Biol. Chem. 270: 15789-15797.PubMedGoogle Scholar
  48. Liddle, S., Keresztessy, Z., Hughes, J. and Hughes, M. A. 1998. A genomic cyanogenic beta-glucosidase gene from Cassava (Accession No. X94986). Plant Physiol. 117: 1526.Google Scholar
  49. Lim, E.-K., Li, Y., Parr, A., Jackson, R., Ashford, D. A. and Bowles, D. J. 2001a. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J. Biol. Chem. 276: 4344-4349.PubMedGoogle Scholar
  50. Lim, E.-K., Doucet, C. J., Li, Y., Elias, L., Worrall, D., Spencer, S. P., Ross, J. and Bowles, D. J. 2001b. The activity of Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates. J. Biol. Chem. 277: 586-592.PubMedGoogle Scholar
  51. Malboobi, M. A, Tremblay, L. and Lefebvre, D. D. 1996. Identification and nucleotide sequences of cDNA clones of phosphate-starvation inducible beta-glucosidase genes of Brassicaceae (Accession nos. U72153 and U72154; Plant Gene Register PGR96-114). Plant Physiol. 112: 1399.Google Scholar
  52. Malboobi, M. A. and Lefebvre, D. D. 1997. A phosphatestarvation inducible beta-glucosidase gene (psr3. 2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol. Biol. 34: 57-68.PubMedGoogle Scholar
  53. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., Dangl, J. L. and Dietrich, R. A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26: 403-410.PubMedGoogle Scholar
  54. Matsushima, R., Kondo, M., Nishimura, M. and Hara-Nishimura, I. 2003a. A novel ER-derived compartment, the ER body, selectively accumulates a b-glucosidase with an ER-retention signal in Arabidopsis. Plant J. 33: 493-502.PubMedGoogle Scholar
  55. Matsushima, R., Hayashi, Y., Yamada, K., Shimada, T., Nishimura, M. and Hara-Nishimura, I. 2003b. The ER body, a novel endoplasmic reticulum-derived structure in Arabidopsis. Plant Cell Physiol. 44: 661-666.PubMedGoogle Scholar
  56. McMahon, J. M. and Sayre, R. T. 1997. Genomic sequence for a linamarase gene from cassava (Manihot esculenta Crantz) (GenBank Accession No. U95298). Direct submission.Google Scholar
  57. Mo, B. and Bewley, J. D. 2002. b-Mannosidase (EC 3. 2. 1. 25) activity during and following germination of tomato (Lycopersicon esculentum Mill. ) seeds. Purification, cloning and characterization. Planta 215: 141-152.PubMedGoogle Scholar
  58. Møller, B. L. and Poulton, J. E. 1993. Cyanogenic glycosides. In: P. J. Lea (Ed. ) Methods in Plant Biochemistry. Vol. 9, Enzymes of secondary metabolism, Academic Press, New York, pp. 183-207.Google Scholar
  59. Mount, S. M. 1982. A catalogue of splice junction sequences. Nucleic Acids Res. 10: 459-472.PubMedGoogle Scholar
  60. Niemeyer, H. M. 1988. Hydroxamic acids (4-hydroxy-1, 4-benzoxazin-3-ones), defense chemicals in the Gramineae. Phytochemistry 27: 3349-3358.Google Scholar
  61. Nikus, J., Esen, A., and Jonsson, L. M. V. 2003. Cloning of a plastidic rye (Secale cereale) b-glucosidase cDNA and its expression in Escherichia coli. Physiol. Plant. 118: 337-345.Google Scholar
  62. Nisius, A. 1988. The stromacentre in Avena plastids: an aggregation of b-glucosidase responsible for the activation of oat-leaf saponins. Planta 173: 474-481.Google Scholar
  63. Nitz, I., Berkefeld, H., Puzio, P. S. and Grundler, F. M. W. 2001. Pyk10, a seedling and root specific gene and promoter from Arabidopsis thaliana. Plant Sci. 161: 337-346.PubMedGoogle Scholar
  64. Piao, H. L. and Hwang, I. 2000. A transgenic Arabidopsis plant overexpressing an ER localized b-glucosidase homolog that is transcriptionally suppressed by NaCl is hypersensitive to NaCl stress (direct sequence submission to GenBank).Google Scholar
  65. Poulton, J. E. 1990. Cyanogenesis in plants. Plant Physiol. 94: 401-405.Google Scholar
  66. Rask, L., Andréasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B. and Meijer, J. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42: 93-113.PubMedGoogle Scholar
  67. Raychaudhuri, A. and Tipton, P. A. 2002. Cloning and expression of the gene for soybean hydroxyisourate hydrolase. Localization and implications for function and mechanism. Plant Physiol. 130: 2061-2068.PubMedGoogle Scholar
  68. Raychaudhuri, A. and Tipton, P. A. 2003. A familiar motif in a new context: the catalytic mechanism of hydroxyisourate hydrolase. Biochemistry 42: 6848-6852.PubMedGoogle Scholar
  69. Reichelt, M., Brown, P. D., Schneider, B., Oldham, N. J., Stauber, E., Tokuhisa, J., Kliebenstein, D. J., Mitchell-Olds, T. and Gershenzon, J. 2002. Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59: 663-671.PubMedGoogle Scholar
  70. Ross, J., Li, Y., Lim, E.-K. and Bowles, D. J. 2001. Higher plant glycosyltransferases. Genome Biol. 2: 1-6.Google Scholar
  71. Rubinelli, P., Hu, Y. and Ma, H. 1998. Identification, sequence analysis and expression studies of novel anther-specific genes of Arabidopsis thaliana. Plant Mol. Biol. 37: 607-619.PubMedGoogle Scholar
  72. Ryan, K. G., Swinny, E. E, Winefield, C. and Markham, K. R. 2001. Flavonoids and UV photoprotection in Arabidopsis mutants. Z. Naturforsch. 56c: 745-754.Google Scholar
  73. Schmidt, K. P., Burrows, P. R., Davies, K. G., Kammerloher. W., Schaeffner, A. R., Buck, F., Cai, D. and Grundler, F. M. W. 1995. A root specific myrosinase in Arabidopsis responding to cyst nematode infection (direct sequence submission to GenBank).Google Scholar
  74. Sharp, P. A. 1981. Speculations on RNA splicing. Cell 23: 643-646.PubMedGoogle Scholar
  75. Simillion, C., Vandepoele, K., Van Montagu, M. C., Zabeau, M. and Van de Peer, Y. 2002. The hidden duplication past of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 99: 13627-13632.PubMedGoogle Scholar
  76. Snyder, M. and Gerstein, M. 2003. Defining genes in the genomics era. Science 300: 258-260.PubMedGoogle Scholar
  77. Stotz, H. U., Pittendrigh, B. R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A. and Mitchell-Olds, T. 2000. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124: 1007-1017.PubMedGoogle Scholar
  78. Thayer, S. S. and Conn, E. E. 1981. Subcellular localization of dhurrin b-glucosidase and hydroxynitrile lyase in the mesophyll cells of Sorghum leaf blades. Plant Physiol. 67: 617-622.Google Scholar
  79. Thorlby, G., Veale, E., Butcher, K. and Warren, G. J. 1999. Map positions of SFR genes in relation to other freezingrelated genes of Arabidopsis thaliana. Plant J. 17: 445-452.PubMedGoogle Scholar
  80. Thorlby, G. J. and Warren, G. J. 2002. The sfr2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a putative beta-glycosidase (direct sequence submission to GenBank).Google Scholar
  81. Veit, M. and Pauli, G. F. 1999. Major flavonoids from Arabidopsis thaliana leaves. J Nat. Prod. 62: 1301-1303.PubMedGoogle Scholar
  82. Verdoucq, L., Moriniere, J., Bevan, D. R., Esen, A., Vasella, A., Henrissat, B. and Czjzek, M. 2004. Structural determinants of substrate specificity in family 1 beta-glucosidases: novel insights from the crystal structure of sorghum dhurrinase-1, a plant beta-glucosidase with strict specificity, in complex with its natural substrate. J. Biol. Chem. (in press).Google Scholar
  83. Vision, T. J., Brown, D. G. and Tanksley, S. D. 2000. The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.PubMedGoogle Scholar
  84. Xue, J. and Rask, L. 1995. The unusual 5' splicing border GC is used in myrosinase genes of the Brassicaceae. Plant Mol. Biol. 29: 167-171.PubMedGoogle Scholar
  85. Xue, J., Jorgensen, M., Pihlgren, U. and Rask, L. 1995. The myrosinase gene family in Arabidopsis thaliana: gene organization, expression and evolution. Plant Mol. Biol. 27: 911-922.PubMedGoogle Scholar
  86. Yoshida, S., Ito, M., Nishida, I. and Watanabe, A. 2001. Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana. Plant Cell Physiol. 42: 170-178.PubMedGoogle Scholar
  87. Zhang, J., Pontoppidan, B., Xue, J., Rask, L. and Meijer, J. 2002. The third myrosinase gene TGG3 in Arabidopsis thaliana is a pseudogene specifically expressed in stamen and petal. Physiol. Plant. 115: 25-34.PubMedGoogle Scholar
  88. Zhong, R. and Ye, Z.-H. 2003. The SAC domain-containing protein gene family in Arabidopsis. Plant Physiol. 132: 544-555.PubMedGoogle Scholar
  89. Zhou, J., Hartmann, S., Shepherd, B. K. and Poulton, J. E. 2002. Investigation of the microheterogeneity and aglycone speci-ficity-conferring residues of black cherry prunasin hydrolases. Plant Physiol. 129: 1252-1264.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Zhiwei Xu
    • 1
    • 2
  • Luis Escamilla-Treviño
    • 1
  • Lihui Zeng
    • 1
    • 3
  • Mallikarjun Lalgondar
    • 4
  • David Bevan
    • 5
  • Brenda Winkel
    • 6
  • Ali Mohamed
    • 7
  • Chi-Lien Cheng
    • 1
  • Ming-Che Shih
    • 1
  • Jonathan Poulton
    • 1
  • Asim Esen
    • 4
  1. 1.Department of Biological SciencesThe University of IowaUSA
  2. 2.Department of Internal MedicineThe University of IowaUSA
  3. 3.College of HorticultureFujian Agriculture and Forestry UniversityFujianPeople's Republic of China
  4. 4.Department of BiologyVirginia Polytechnic Institute and State UniversityUSA
  5. 5.Biochemistry DepartmentVirginia Polytechnic Institute and State UniversityUSA
  6. 6.Fralin Biotechnology CenterVirginia Polytechnic Institute and State UniversityUSA
  7. 7.Department of BiologyVirginia State UniversityUSA

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