Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana

Plant and Cell Physiology

Volumn 49, Issue 9, 2008, Pages 1331-1341

  Eudes, Aymerick ^a,b   Mouille, Grégory ^a   Thévenin, Johanne ^a   Goyallon, Arnaud ^a   Minic, Zoran ^a   Jouanin, Lise ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Arabidopsis; Arabinogalactan protein; Beta glucuronidase; Family 79 glycoside hydrolase; Hypocotyl and root growth

Indexed keywords

ARABIDOPSIS PROTEIN; ARABINOGALACTAN PROTEINS; BETA GLUCURONIDASE; GLUCURONIC ACID; MUCOPROTEIN; PLANT RNA; POLYSACCHARIDE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHROMATOGRAPHY; ENZYMOLOGY; GENE; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PH; PLANT GROWTH; PLANT ROOT; TEMPERATURE; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY; CLONING, MOLECULAR; GENES, PLANT; GLUCURONIC ACID; GLUCURONIDASE; HYDROGEN-ION CONCENTRATION; HYPOCOTYL; MOLECULAR SEQUENCE DATA; MUCOPROTEINS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; RNA, PLANT; TEMPERATURE; TRANSFORMATION, GENETIC;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; FUNGI; MAMMALIA;

EID: 51749117193     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcn108     Document Type: Article

References (61)

1. Alwen, A., Benito Moreno, R.M., Vicente, O. and Heberle-Bors, E. (1992) Plant endogenous beta-glucuronidase activity: how to avoid interference with the use of the E. coli beta-glucuronidase as a reporter gene in transgenic plants. Transgenic Res. 1: 63-70.
2. Barth, C. and Jander, G. (2006) Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J. 46: 549-562.
3. Bayer, E.M., Bottrill, A.R, Walshaw, J., Vigouroux, M., Naldrett, M.J., Thomas, C.L. and Maule, A.J. (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6: 301-311.
4. Bendtsen, J.D., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783-795.
5. Betchold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82: 259-266.
6. Boudart, G., Jamet, E., Rossignol, M., Lafitte, C., Borderies, G., Jauneau, A., Esquerre-Tugaye, M.T. and Pont-Lezica, R. (2005) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5: 212-221.
7. Bradford, N.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
8. Burton, R.A., Gibeaut, D.M., Bacic, A., Findlay, K., Roberts, K., Hamilton, A., Baulcombe, D.C. and Fincher, G.B. (2000) Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12: 691-706.
9. Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005-1016.
10. Escamilla-Trevino, L.L., Chen, W., Card, M.L., Shih, M.C., Cheng, C.L. and Poulton, J.E. (2006) Arabidopsis thaliana beta-Glucosidases BGLU45 and BGLU46 hydrolyse monolignol glucosides. Phytochemistry 671: 651-660.
11. Estelle, M. and Somerville, C. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206: 200-206.
12. Etzler, M.E. (1998) Oligosaccharide signaling of plant cells. J. Cell. Biochem. Suppl. 30-31: 123-128.
13. Falquet, L., Pagni, M., Bucher, P., Hulo, N., Sigrist, C.J., Hofmann, K. and Bairoch, A. (2002) The PROSITE database, its status in 2002. Nucleic Acids Res. 30: 235-238.
14. Fincher, G.B., Stone, B.A. and Clarke, A.E. (1983) Arabinogalactan- proteins: structure, biosynthesis, and function. Annu. Rev. Plant Physiol. 34: 47-70.
15. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M. and Höfte, H. (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114: 295-305.
16. Gibeaut, D.M. and Carpita, N.C. (1991) Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol. 97: 551-561.
17. Grignon, C. and Sentenac, H. (1991) pH and ionic conditions in the apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 103-128.
18. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280: 309-316.
19. Hodal, L., Bochardt, A., Nielsen, J.E., Mattsson, O. and Okkels, F.T. (1992) Detection, expression and specific elimination of endogenous β-glucuronidase activity in transgenic and non-transgenic plants. Plant Sci. 87: 115-122.
20. Hu, C.Y., Chee, P.P., Chesney, R.H., Zhou, J.H., Miller, P.D. and O'Brien, W.T. (1990) Intrinsic GUS-like activities in seed plants. Plant Cell Rep. 9: 1-5.
21. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
22. Kim, J.-B. and Carpita, N.C. (1992) Changes in esterification of the uronic acids groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol. 98: 646-653.
23. Koncz, C. and Schell, J. (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204: 383-338.
24. Konishi, T., Kotake, T., Soraya, D., Matsuoka, K., Koyama, T., Kaneko, S., Igarashi, K., Samejima, M. and Tsumuraya, Y. (2008) Properties of family 79 beta-glucuronidases that hydrolyze betaglucuronosyl and 4-O-methyl-beta- glucuronosyl residues of arabinogalactan-protein. Carbohydr. Res. 343: 1191-1201.
25. Kotake, T., Dina, S., Konishi, T., Kaneko, S., Igarashi, K., Samejima, M., Watanabe, Y., Kimura, K. and Tsumuraya, Y. (2005) Molecular cloning of a β-galactosidase from radish that specifically hydrolyzes β-(1→3)-and β-(1→6)-galactosyl residues of arabinogalactan protein. Plant Physiol. 138: 1563-1576.
26. Kotake, T., Tsuchiya, K., Aohara, T., Konishi, T., Kaneko, S., Igarashi, K., Samejima, M. and Tsumuraya, Y. (2006) An alpha-L-arabinofuranosidase/beta-D- xylosidase from immature seeds of radish (Raphanus sativus L.). J. Exp. Bot. 57: 2353-2362.
27. Laemmli, U.K. (1970) Cleavage of the structural proteins during the assembly of the head of the bacteriophage T4. Nature 227: 680-685.
28. Lee, K.H., Piao, H.L., Kim, H-Y., Choi, S.M., Jiang, F., Hartung, W., Hwang, I., Kwak, J.M., Lee, I.-J. and Hwang, I. (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126: 1109-1120.
29. Ma, P., Beck, S.L., Raab, R.W., McKown, R.L., Coffman, G.L., Utani, A., Chirico, W.J., Rapraeger, A.C. and Laurie, G.W. (2006) Heparanase deglycanation of syndecan-1 is required for binding of the epithelial-restricted prosecretory mitogen lacritin. J. Cell Biol. 174: 1097-1106.
30. Marchler-Bauer, A., Anderson, J.B., Cherukuri, P.F., DeWeese-Scott, C., Geer, L.Y., et al. (2005) CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res. 33(Database Issue): D192-196.
31. Minic, Z., Do, C.-T., Rihouey, C., Morin, H., Lerouge, P. and Jouanin, L. (2006) Purification, functional characterization, cloning, and identification of mutants of a seed-specific arabinan hydrolase in Arabidopsis. J. Exp. Bot. 57: 2339-2351.
32. Minic, Z. and Jouanin, L. (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol. Biochem. 44: 435-449.
33. Minic, Z., Jamet, E., Negroni, L., Arsene der Garabedian, P., Zivy, M. and Jouanin, L. (2007) A sub-proteome of Arabidopsis thaliana mature stems trapped on Concanavalin A is enriched in cell wall glycoside hydrolases. J. Exp. Bot. 58: 2503-2512.
34. Morimoto, S., Harioka, T. and Shoyama, Y. (1995) Purification and characterization of flavone-specific β-glucuronidase from callus cultures of Scutellaria baicalensis Georgi. Planta 195: 535-540.
35. Motose, H., Sugiyama, M. and Fukuda, H. (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873-878.
36. Nesi, N., Debeaujon, I., Jond, C., Stewart, A.J., Jenkins, G.I., Caboche, M. and Lepiniec, L. (2002) The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14: 2463-2479.
37. Nothnagel, E.A. (1997) Proteoglycans and released components in plant cells. Int. Rev. Cytol. 174: 195-291.
38. O'Leary, K.A., Day, A.J., Needs, P.W., Sly, W.S., O'Brien, N.M. and Williamson, G. (2001) Flavonoid glucuronides are substrates for human liver beta-glucuronidase. FEBS Lett. 503: 103-106.
39. Plegt, L. and Bino, R.J. (1989) β-glucuronidase activity during development of the male gametophyte from transgenic and non-transgenic plants. Mol. Gen. Genet. 216: 321-327.
40. Ray, J., Scarpino, V., Laing, C. and Haskins, M.E. (1999) Biochemical basis of the beta-glucuronidase gene defect causing canine mucopolysaccharidosis VII. J. Hered. 90: 119-123.
41. Sambrook, J., Fritsch, E. and Manaiatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
42. Santoni, V., Vinh, J., Pflieger, D., Sommerer, N. and Maurel, C. (2003) A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem. J. 373: 289-296.
43. Sasaki, K., Taura, F., Shoyama, Y. and Morimoto, S. (2000) Molecular characterization of a novel beta-glucuronidase from Scutellaria baicalensis Georgi. J. Biol. Chem. 275: 27466-27472.
44. Sasaki, N., Higashi, N., Taka, T., Nakajima, M. and Irimura, T. (2004) Cell surface localization of heparanase on macrophages regulates degradation of extracellular matrix heparan sulfate. J. Immunol. 172: 3830-3835.
45. Schultz, C.J., Johnson, K.L., Currie, G. and Bacic, A. (2000) The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12: 1751-1768.
46. Schulz, M. and Weissenböck, G. (1987) Partial purification and characterization of a luteolin-triglucuronide-specific β-glucuronidase from rye primary leaves (Secale cereale). Phytochemistry 26: 933-937.
47. Seifert, G.J., Barber, C., Wells, B., Dolan, L. and Roberts, K. (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr. Biol. 21: 1840-1845.
48. Serpe, M.D. and Nothnagel, E.A. (1995) Fractionation and structural characterization of arabinogalactan-proteins from the cell wall of rose cells. Plant Physiol. 109: 1007-1016.
49. Showalter, A.M. (2001) Arabinogalactan-proteins: structure, expression and function. Cell. Mol. Life Sci. 58: 1399-1417.
50. Sood, P.P. (1980) Histoenzymological compartmentation of β-glucuronidase in the germinating pollen grains of Portulaca grandiflora. Biol. Plant. 22: 124-127.
51. Sudan, C., Prakash, S., Bhomkar, P., Jain, S. and Bhalla-Sarin, N. (2006) Ubiquitous presence of beta-glucuronidase (GUS) in plants and its regulation in some model plants. Planta 224: 853-854.
52. Takeda, T. and Fry, S.C. (2004) Control of xyloglucan endotransglucosylase activity by salts and anionic polymers. Planta 219: 722-732.
53. Takeuchi, Y. and Komamine, A. (1980) Turnover of cell wall polysaccharides of a Vinca rosea suspension culture. III. Turnover of arabinogalactan. Physiol. Plant. 50: 113-118.
54. Tohyama, O., Imura, A., Iwano, A., Freund, J.N., Henrissat, B., Fujimori, T. and Nabeshima, Y. (2004) Klotho is a novel beta-glucuronidase capable of hydrolyzing steroid beta-glucuronides. J. Biol. Chem. 279: 9777-9784.
55. van Hengel, A.J., Tadesse, Z., Immerzeel, P., Schols, H., van Kammen, A. and de Vries, S.C. (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol. 125: 1880-1890.
56. van Hengel, A.J. and Roberts, K. (2002) Fucosylated arabinogalactan- proteins are required for full root cell elongation in Arabidopsis. Plant J. 32: 105-113.
57. van Hengel, A.J., van Kammen, A. and De Vries, S.C. (2002) A relationship between seed development, Arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol. Plant. 114: 637-634.
58. Wenzl, P., Wong, L., Kwang-won, K. and Jefferson, R.A. (2005) A functional screen identifies lateral transfer of beta-glucuronidase (gus) from bacteria to fungi. Mol. Biol. Evol. 22: 308-316.
59. Willats, W.G. and Knox, J.P. (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of beta-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J. 9: 919-925.
60. Woo, H.H., Jeong, B.R., Hirsch, A.M. and Hawes, M.C. (2007) Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. Genomics 90: 143-153.
61. Xu, X., Rao, G., Quiros, R.M., Kim, A.W., Miao, H.Q., Brunn, G.J., Platt, J.L., Gattuso, P. and Prinz, R.A. (2007) In vivo and in vitro degradation of heparan sulfate (HS) proteoglycans by heparanase-1 (HPR1) in pancreatic adenocarcinomas: Loss of cell surface HS suppresses FGF2-mediated cell signaling and proliferation. J. Biol. Chem. 282: 2363-2373.