Identification of the first Oomycete annexin as a (1→3)-β-D- glucan synthase activator

Molecular Microbiology

Volumn 62, Issue 2, 2006, Pages 552-565

  Bouzenzana, Jamel ^a   Pelosi, Ludovic ^b,c   Briolay, Anne ^a   Briolay, Jérôme ^a   Bulone, Vincent ^a,d  

^a UNIVERSITÉ LYON 1   (France)

^b CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^c CEA GRENOBLE   (France)

^d ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 BETA GLUCAN SYNTHASE; ANNEXIN;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OOMYCETES; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANNEXINS; BLOTTING, WESTERN; CALCIUM CHLORIDE; CATALYSIS; DNA, COMPLEMENTARY; EGTAZIC ACID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLUCOSYLTRANSFERASES; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; OOMYCETES; PHYLOGENY; SAPROLEGNIA; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID;

OOMYCETES; SAPROLEGNIA MONOICA;

EID: 33749178253     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05389.x     Document Type: Article

References (59)

1. Andrawis, A., Solomon, M., and Delmer, D.P. (1993) Cotton fiber annexins: a potential role in the regulation of callose synthase. Plant J 3: 763-772.
2. Aronson, J.M., and Lin, C.C. (1978) Hyphal cell wall chemistry of Leptomitus lacteus. Mycologia 70: 363-369.
3. Baldauf, S.L., Roger, A.J., Wenk-Siefert, I., and Doolittle, W.F. (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972-977.
4. Bandorowicz-Pikula, J., Buchet, R., and Pikula, S. (2001) Annexins as nucleotide-binding proteins: facts and speculations. Bioessays 23: 170-178.
5. Bartnicki-Garcia, S. (1968) Cell wall chemistry, morphogenesis and taxonomy of fungi. Annu Rev Microbiol 22: 87-108.
6. Barton, G.J., Newman, R.H., Freemont, P.S., and Crumpton, M.J. (1991) Amino acid sequence analysis of the annexin super-gene family of proteins. Eur J Biochem 198: 749-760.
7. Beauvais, A., Bruneau, J.M., Mol, P.C., Buitrago, M.J., Legrand, R., and Latgé, J.P. (2001) Glucan synthase complex of Aspergillus fumigatus. J Bacteriol 183: 2273-2279.
8. Billon-Grand, G., Marais, M.-F., Joseleau, J.-P., Girard, V., Gay, L., and Fèvre, M. (1997) A novel (1→3)-β-glucan synthase from the Oomycete Saprolegnia monoica. Microbiology 143: 3175-3183.
9. Blum, H., Beier, H., and Gross, H. (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93-99.
10. Boustead, C.M., Smallwood, M., Small, H., Bowles, D.J., and Walker, J.H. (1989) Identification of calcium-dependent phospholipid-binding proteins in higher plant cells. FEBS Lett 244: 456-460.
11. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
12. Braun, E.L., Kang, S., Nelson, M.A., and Natvig, D.O. (1998) Identification of the first fungal annexin: analysis of annexin gene duplications and implications for eukaryotic evolution. J Mol Evol 47: 531-543.
13. Bulone, V., and Fèvre, M. (1996) A 34-kDa polypeptide is associated with (1→3)-β-glucan synthase activity from the fungus Saprolegnia monoica. FEMS Microbiol Lett 140: 145-150.
14. Bulone, V., Girard, V., and Fèvre, M. (1990) Separation and partial purification of (1→3)-β-glucan and (1→4)-β-glucan synthases from Saprolegnia. Plant Physiol 94: 1748-1755.
15. Bulone, V., Chanzy, H., Gay, L., Girard, V., and Fèvre, M. (1992) Characterization of chitin and chitin synthase from the cellulosic cell wall fungus Saprolegnia monoica. Exp Mycol 16: 8-21.
16. Bulone, V., Fincher, G.B., and Stone, B.A. (1995) In vitro synthesis of a microfibrillar (1→3)-β-glucan by a ryegrass (Lolium multiflorum) endosperm (1→3)-β-glucan synthase enriched by product entrapment. Plant J 8: 213-225.
17. Burgoyne, R.D., and Geisow, M.J. (1989) The annexin family of calcium-binding proteins. Cell Calcium 10: 1-10.
18. Calvert, C.M., Gant, S.J., and Bowles, D.J. (1996) Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell 8: 333-342.
19. Campos-Takaki, G.M., Dietrich, S.M.C., and Mascarenhas, Y. (1982) Isolation and characterization of chitin from the cell walls of Achlya radiosa. J Gen Microbiol 128: 207-209.
20. Chen, J.M., Sheldon, A., and Pincus, M.R. (1993) Structure-function correlations of calcium binding and calcium channel activities based on 3-dimensional models of human annexins I, II, III, V and VII. J Biomol Struct Dyn 10: 1067-1089.
21. Delmer, D.P. (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50: 245-276.
22. Delmer, D.P., and Potikha, T.S. (1997) Structures and functions of annexins in plants. Cell Mol Life Sci 53: 546-553.
23. Doblin, M.S., Kurek, I., Jacob-Wilk, D., and Delmer, D.P. (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43: 1407-1420.
24. Douglas, C.M., Foor, F., Marrinan, J.A., Morin, N., Nielsen, J.B., Dahl, A.M., et al. (1994) The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of (1→3)-β-glucan synthase. Proc Natl Acad Sci USA 91: 12907-12911.
25. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
26. Fèvre, M. (1983) Nucleotide effects on glucan-synthesis activities of particulate enzymes from Saprolegnia. Planta 159: 130-135.
27. Fry, W.E., and Goodwin, S.B. (1997a) Re-emergence of potato and tomato late blight in the United States. Plant Dis 81: 1349-1357.
28. Fry, W.E., and Goodwin, S.B. (1997b) Resurgence of the Irish potato famine fungus. Bioscience 47: 363-371.
29. Gajendran, K., Gonzales, M.D., Farmer, A., Archuleta, E., Win, J., Waugh, M.E., and Kamoun, S. (2006) Phytophthora functional genomics database (PFGD): functional genomics of phytophthora-plant interactions. Nucleic Acids Res 34: D465-D470.
30. Galtier, N., Gouy, M., and Gautier, C. (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548.
31. Geisow, M., Fritsche, U., Hexham, J., Dash, B., and Johnson, T.A. (1986) A consensus amino acid sequence repeat in Torpedo and mammalian calcium-dependent membrane binding proteins. Nature 320: 636-638.
32. Gerke, V., and Moss, S.E. (2002) Annexins: from structure to function. Physiol Rev 82: 331-371.
33. Girard, V., and Fèvre, M. (1991) Solubilization of a membrane-bound stimulator of (1→3)-β-glucan synthase from Saprolegnia. Plant Sci 76: 193-200.
34. Hofmann, A. (2004) Annexins in the plant kingdoms. Annexins 1: 51-61.
35. Hofmann, A., Delmer, D.P., and Wlodawer, A. (2003) The crystal structure of annexin Gh1 from Gossypium hirsutum reveals an unusual S3 cluster. Eur J Biochem 270: 2557-2564.
36. Johnson, T.W., Jr, Seymour, R.L., and Padgett, D.E. (2002) Biology and Systematics of the Saprolegniaceae. Book published on the World-Wide-Web: http://dl.uncw.edu
37. Khalaj, V., Smith, L., Brookman, J., and Tuckwell, D. (2004) Identification of a novel class of annexin genes. FEBS Lett 562: 79-86.
38. Kumar, C., and Rzhetsky, A. (1996) Evolutionary relationships of eukaryotic kingdoms. J Mol Evol 42: 183-193.
39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
40. Lartseva, L.V. (1986) Saprolegnia on the spawn of sturgeons and salmons. Hydrobiol J 22: 103-107.
41. Li, J., Burton, R.A., Harvey, A.J., Hrmova, M., Wardak, A.Z., Stone, B.A., and Fincher, G.B. (2003) Biochemical evidence linking a putative callose synthase gene with (1→3)-β-D-glucan biosynthesis in barley. Plant Mol Biol 53: 213-225.
42. Lin, C.C., and Aronson, J.M. (1970) Chitin and cellulose in the cell walls of the Oomycete Apodachlya sp. Arch Mikrobiol 72: 111-114.
43. McClung, A.D., Carroll, A.D., and Battey, N.H. (1994) Identification and characterization of ATPase activity associated with maize (Zea mays) annexins. Biochem J 303: 709-712.
44. Machlis, L. (1953) Growth and nutrition of watermolds in the subgenus Euallomyces. II - optimal composition of the minimal medium. Am J Bot 40: 449-460.
45. Margulis, L., and Schwartz, K.V. (2000) Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth. New York, NY: Freeman and Co.
46. Matsudaira, P. (1993) A Practical Guide to Protein and Peptide Purification for Microsequencing. San Diego: Academic Press.
47. Mazur, P., and Baginsky, W. (1996) In vitro activity of (1→3)-β-glucan synthase requires the GTP-binding protein Rho1. J Biol Chem 271: 14604-14609.
48. Neish, G.A., and Hughes, G.C. (1980) Fungal Diseases of Fishes, Book 6. Neptune, NJ: T.W.F. Publications.
49. Paquin, B., Laforest, M.J., Forget, L., Roewer, I., Wang, Z., Longcore, J., and Lang, B.F. (1997) The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 31: 380-395.
50. Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P., and Stalker, D.M. (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci USA 93: 12637-12642.
51. Pelosi, L., Imai, T., Chanzy, H., Heux, L., Buhler, E., and Bulone, V. (2003) Structural and morphological diversity of (1→3)-β-D-glucans synthesized in vitro by enzymes from Saprolegnia monoica. Comparison with a corresponding in vitro product from blackberry (Rubus fruticosus). Biochemistry 42: 6264-6274.
52. Qadota, H., Python, C.P., Inoue, S.B., Arisawa, M., Anraku, Y., Zheng, Y., et al. (1996) Identification of yeast Rho1p GTPase as a regulatory subunit of (1→3)-β-glucan synthase. Science 272: 279-281.
53. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
54. Shematek, E.M., and Cabib, E. (1980) Biosynthesis of the yeast cell wall. II. Regulation of (1→3)-β-glucan synthetase by ATP and GTP. J Biol Chem 255: 895-902.
55. Shin, H., and Brown, R.M., Jr (1999) GTPase activity and biochemical characterization of a recombinant cotton fiber annexin. Plant Physiol 119: 925-934.
56. Smallwood, M.F., Gurr, S.J., McPherson, M.J., Roberts, K., and Bowles, D.J. (1990) Purification and partial sequence analysis of plant annexins. Biochem J 281: 501-505.
57. Thompson, J., Higgins, D., and Gibson, T. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
58. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases, and other ATP-requiring enzymes and a common nucleotide-binding fold. EMBO J 1: 945-951.
59. Wessels, J.G.H., and Sietsma, J.H. (1981) Fungal cell walls: a survey. In Encyclopedia of Plant Physiology. Plant Carbohydrates II. Tanner, W., and Loewus, F.A., (eds). Berlin: Springer Verlag, pp. 352-394.