Cloning and characterization of 1,3-β-glucanase-encoding genes from non-conventional yeasts

Yeast

Volumn 15, Issue 2, 1999, Pages 91-109

  Esteban, Pedro F ^a   Vazquez De Aldana, Carlos R ^a   Del Rey, Francisco ^a,b  

^a Instituto de Biología Funcional y Genómica and Departamento de Microbiología y Genética   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

1,3 glucanase; Hansenula; HpEXG1; KlEXG1; Kluyveromyces; Schwanniomyces; SoEXG1

Indexed keywords

1,3 BETA GLUCANASE; GLYCOSIDASE; OLIGONUCLEOTIDE; POLYPEPTIDE;

ARTICLE; CONTROLLED STUDY; DNA PROBE; ENZYME RELEASE; ENZYME SPECIFICITY; FUNGAL GENETICS; GENE EXPRESSION; GENE LIBRARY; HANSENULA POLYMORPHA; KLUYVEROMYCES; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FAMILY; PROTEIN GLYCOSYLATION; SACCHAROMYCES CEREVISIAE; YEAST;

DEBARYOMYCES; DEBARYOMYCES OCCIDENTALIS; HANSENULA POLYMORPHA; KLUYVEROMYCES; KLUYVEROMYCES LACTIS; PICHIA; PICHIA ANGUSTA; SACCHAROMYCES CEREVISIAE; SCHWANNIOMYCES OCCIDENTALIS;

EID: 0033616383     PISSN: 0749503X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1097-0061(19990130)15:2<91::aid-yea343>3.0.co;2-%23     Document Type: Article

References (85)

1. Abd-El-Al, A. T. H. and Phaff, H. J. (1968). Exo-β-glucanases in yeast. Biochem. J. 109, 347-360.
2. Baird, S. D., Hefford, M. A., Johnson, D. A., Sung, W. L., Yaguchi, M. and Seligy, V. L. (1990). The Glu residue in the conserved Asn-Glu-Pro sequence of two highly divergent endo-β-1,4-glucanases is essential for enzymatic activity. Biochem. Biophys. Res. Commun. 169, 1035-1039.
3. Baker, R. (1991). Rapid colony transformation of Saccharomyces cerevisiae. Nucl. Acids Res. 19, 1945.
4. Ballou, C. E. (1982). Yeast cell wall and cell surface. In Strathern, J. N., Jones, E. W. and Broach, J. R. (Eds), The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression. Cold Spring Harbor Laboratory Press, New York, pp. 335-360.
5. Bennetzen, J. L. and Hall, B. D. (1982). The primary structure of the Saccharomyces cerevisiae gene for alcohol dehydrogenase I. J. Biol. Chem. 257, 3018-3025.
6. Borck, J., Beggs, J. D., Brammer, W. J., Hopkins, A. S. and Murray, N. E. (1976). The construction in vitro of transducing derivatives of phage lambda. Mol. Gen. Genet. 146, 199-207.
7. Bortoli-German, I., Haiech, J., Chippaux, M. and Barras, F. (1995). Informational suppression to investigate structural functional and evolutionary aspects of the Erwinia chrysanthemi cellulase EGZ. J. Mol. Biol. 246, 82-94.
8. Brener, C. and Fuller, R. S. (1992). Structural and enzymatic characterization of a purified prohormone-processing enzyme: secreted, soluble Kex2 protease. Proc. Natl Acad. Sci. USA 89, 922-926.
9. Bussey, H. (1988). Proteases and the processing of precursors to secreted proteins in yeast. Yeast 4, 17-26.
10. Carmichael, G. G. and McMaster, G. K. (1980). The analysis of nucleic acids in gel using glyoxal and acridine orange. Methods Enzymol. 65, 380-391.
11. Chambers, R. S., Broughton, M. J., Cannon, R. D., Carne, A., Emerson, G. W. and Sullivan, P. A. (1993a). An exo-β-(1,3)-glucanase of Candida albicans: purification of the enzyme and molecular cloning of the gene. J. Gen. Microbiol 139, 325-334.
12. Chambers, R. S., Waiden, A. R., Brooke, G. S., Cutfield, J. F. and Sullivan, P. A. (1993b). Identification of a putative active site residue in the exo-β-(1,3)-glucanase of Candida albicans. FEBS Lett. 3, 366-369.
13. Christianson, W. T., Sikorski, R. S., Dante, M., Shero, J. H. and Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
14. Cid, V., Durán, A., del Rey, F., Snyder, M. P., Nombela, C. and Sánchez, M. (1995). Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol. Rev. 59, 345-386.
15. Correa, J. (1993). Caracterización del gen EXG2 de Saccharomyces cerevisiae. Doctoral thesis. Universidad de Salamanca, Spain.
16. Correa, J., Vazquez de Aldana, C. R., San Segundo, P. and del Rey, F. (1992). Genetic mapping of 1,3-β-glucanase-encoding genes in Saccharomyces cerevisiae, Curr. Genet. 22, 238-288.
17. de la Cruz, J., Pintor-Toro, J. A., Benitez, T., Llobell, A. and Romero, L. C. (1995). A novel endo-β-1,3-glucanase, BGN13.1, involved in the mycoparasitism of Trichoderma harzianum, J. Bacteriol. 177, 6937-6945.
18. del Rey, F., Santos, T., Garcia-Acha, I. and Nombela, C. (1980). Synthesis of 1,3-β-glucanases during sporulation in Saccharomyces cerevisiae: formation of a new sporulation-specific 1,3-β-glucanase. J. Bacteriol. 143, 621-627.
19. Dominguez, R., Souchon, H., Spinelli, S., Dauter, Z., Wilson, K. S., Chauvaux, S., Béguin, P. and Alzari, P. M. (1995). A common protein fold and similar active site in two distinct families of β-glycanases. Nature Struct. Biol. 2, 569-576.
20. Ducros, V., Czjzek, M., Belaich, J.-P., Davies, G. J. and Haser, R. (1995). Crystal structure of the catalytic domain of a bacterial cellulase belonging to family 5. Structure 3, 939-949.
21. Feinberg, A. P. and Vogelstein, B. (1983). A technique for radiolabelling restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
22. Fincher, G. B., Lock, P. A., Morgan, M. M., Lingelbach, K., Wettenhall, R. E. H., Mercer, J. F. B., Barndt, A. and Thomsen, K. K. (1986). Primary structure of the (1-3,1-4)-β-D-glucan 4-glucohydrolase from barley aleurone. Proc. Natl Acad. Sci. USA 83, 2081-2085.
23. Fleet, G. H. (1984). The occurrence and function of endogenous wall-degrading enzymes in yeasts. In Nombela, C. (Ed.), Microbial Cell Wall Synthesis and Autolysis. Elsevier Science Publishers, Amsterdam, pp. 227-238.
24. Hahn, S., Hoar, E. T. and Guarente, L. (1985). Each of three 'TATA elements' specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 82, 8562-8566.
25. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580.
26. Henikoff, S. (1984). Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28, 351-359.
27. Henrissat, B. (1991). A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316.
28. Henrissat, B. and Bairoch, A. (1993). New families in the classification of glycosyl hydrolase based on amino sequence similarities. Biochem. J. 293, 781-788.
29. Henrissat, B., Claeyssens, M., Tomme, P., Lemesle, L. and Mornon, J. P. (1989). Cellulase families revealed by Hydrophobic cluster analysis. Gene 81, 83-95.
30. Higgins, D. G. and Sharp, P. M. (1988). CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73, 237-244.
31. Hubbard, S. C. and Ivatt, R. J. (1981). Synthesis and processing of asparagine-linked oligosaccharides. Anna. Rev. Biochem. 50, 555-583.
32. Ito, H., Fukuda, K., Murata, K. and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
33. Klebl, F. and Tanner, W. (1989). Molecular cloning of a cell wall exo-β-1,3-glucanases from Saccharomyces cerevisiae. J. Bacteriol. 171, 6259-6264.
34. Kozak, M. (1981). Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucl. Acids Res. 9, 5233-5252.
35. Kozak, M. (1989). The scanning model for translation: an update. J. Cell. Biol. 108, 229-241.
36. Kozak, M. (1995). Adherence to the first-AUG rule when a second AUG codon follows closely upon the first. Proc. Natl Acad Sci. USA 92, 2662-2666.
37. Kuranda, M. J. and Robbins, P. W. (1987). Cloning and heterologous expression of glycosidase genes from Saccharomyces cererisiae. Proc. Natl Acad. Sci. USA 84, 2585-2589.
38. Kyte, J. and Doolittle, R. F. (1982). A simple method for displaying the hydrophobic character of a protein. J. Mol. Biol. 157, 105-132.
39. Lachance, M. A., Villa, T. G. and Phaff, H. J. (1977). Purification and partial characterization of a exo-β-glucanase from the yeast Kluyveromyces aestuarii. Can. J. Biochem. 55, 1001-1006.
40. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. Luna-Arias, J. P., Andaluz, E., Ridruejo. J. C., Olivero, I. and Larriba, G. (1991). The major exoglucanase from Candida albicans: a non-glycosylated secretory monomer related to its counterpart from Saccharomyces cerevisiae. Yeast 7, 833-841.
42. Macarrón, R., van Beeumen, J., Henrissat, B., de la Mata, I. and Claeyssens, M. (1993). Identification of an essential glutamate residue in the active site of endoglucanase III from Trichoderma reesei. FEBS Lett. 2, 137-140.
43. Mackenzie, L. F., Brooke, G. S., Cutfield, J. F., Sullivan, P. A. and Withers, S. G. (1997). Identification of Glu-330 as the catalytic nucleophile of Candida albicans exo-β-(1,3)-glucanase. J. Biol. Chem. 272, 3161-3167.
44. Molina, M., Cenamor, R., Sanchez, M. and Nombela, C. (1989). Purification and some properties of Candida albicans exo-1,3-β-glucanase. J. Gen. Microbiol. 135, 309-314.
45. Morrisey, J. H. (1981). Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal. Biochem. 117, 307-310.
46. Mrsa, V., Klebl, F. and Tanner, W. (1993). Purification and characterization of the Saccharomyces cerevisiae BGL2 product, a cell wall endo-β-1,3-glucanase. J. Bacteriol. 175, 2102-2106.
47. Muthukumar, G., Suhng, S. H., Magee, P. T., Jewell, R. D. and Primerano, D. A. (1993). The Saccharomyces cerevisiae SPR1 gene encodes a sporulation-specific exo-1,3-β-glucanase which contributes to ascospore thermotolerance. J. Bacteriol. 175, 386-394.
48. Navas, J. and Béguin, P. (1992). Site-directed mutagenesis of conserved residues of Clostridium thermocellum endoglucanase CelC. Biochem. Biophys. Res. Commun. 189, 807-812.
49. Nebreda, A. R., Vazquez de Aldana, C. R., Villa, T. G., Villanueva, J. R. and del Rey, F. (1987). Heterogeneous glycosylation of the EXG1 gene accounts for the two extracellular exo-β-glucanase from Saccharomyces cerevisiae. FEBS Lett. 220, 27-30.
50. Nebreda, A. R., Villa, T. G., Villanueva, J. R. and del Rey, F. (1986). Cloning of genes related to exo-β-glucanase production by Saccharomyces cerevisiae: characterization of an exo-β-glucanase structural gene. Gene 47, 245-259.
51. Nelson, M. J. (1957). Colorimetric analysis of sugars. Methods Enzymol. 3, 85-86.
52. Nombela, C., Molina, M., Cenamor, R. and Sánchez, M. (1988). Yeast β-glucanases, a complex system of secreted enzymes. Microbiol. Sci. 5, 328-332.
53. Notario, V., Villa, T. G., Benitez, T. and Villanueva, J. R. (1975). β-Glucanases in the yeast Cryptococcus albidus var aerius. Production and separation of β-glucanases in a synchronous culture. Can. J. Microbiol. 22, 261-268.
54. Notario, V., Villa, T. G. and Villanueva, J. R. (1976). Purification of an exo-β-D-glucanase from cell-free extracts of Candida utilis. Biochem. J. 159, 555-562.
55. Percival-Smith, A. and Segall, J. (1986). Characterization and mutational analysis of a cluster of three genes expressed preferentially during sporulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 4, 142-150.
56. Peterson, G. L. (1977). A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83, 346-356.
57. Ponticelli, A. S. and Struhl, K. (1990). Analysis of Saccharomyces cerevisiac his3 transcription in vitro: biochemical support for multiple mechanisms of transcription. Mol. Cell. Biol. 10, 2832-2839.
58. Proudfoot, N. J. and Brownlee, G. G. (1976). 3′ noncoding region sequences in eukaryotic messenger RNA. Nature 263, 211-214.
59. Py, B., Bortoli-German, I., Haiech, J., Chippaux, M. and Barras, F. (1991). Cellulase EGZ of Erwinia chrysanthemi, structural organization and importance of His98 and Glu133 residues for catalysis. Prot. Eng. 4, 325-333.
60. Ram, S. P., Romana, L. K., Shepherd, M. G. and Sullivan, P. A. (1984). Exo-1,3-β-glucanase, autolysin and trehalase activities during yeast growth and germ tube formation in Candida albicans. J. Gen. Microbiol. 130, 1227-1236.
61. Ramirez, M., Hernández, L. M. and Larriba, G. (1989). A similar protein portion for two exoglucanases secreted by Saccharomyces cerevisiae. Arch. Microbiol. 151, 391-398.
62. Rothstein, R. (1983). One-step gene replacement in yeast. Methods Enzymol. 101, 202-211.
63. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
64. San Segundo, P., Correa, J., Vazquez de Aldana, C. R. and Rey, F. del. (1993). SSGI, a gene encoding a sporulation-specific 1,3-β-glucanase in Saccharomyces cerevisiae. J. Bacteriol. 175, 3823-3837.
65. Sanger, F., Nicklen, S. and Coulson, A. R. (1977). DNA sequencing with chain terminating inhibitors. Proc. Natl Acad. Sci. USA 74, 5463-5467.
66. Schaeffer, H. J., Leykam, J. and Walton, J. D. (1994). Cloning and targeted gene disruption of EXG1, encoding exo-β-1,3-glucanase, in the phytopathogenic fungus Cochliobolus carbonum. Appl. Environ. Microbiol. 60, 594-598.
67. Smeekens, S. P. (1993). Processing of protein precursors by a novel family of subtilisin-related mammalian endoproteases. BioTechnology 11, 182-186.
68. Sherman, F., Fink, G. R. and Hicks, J. B. (1986). Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, New York.
69. Shinsi, H., Wenzler, H., Neuhaus, J. M., Felix, G., Hofsteenge, J. and Meins, F., Jr (1988). Evidence for N- and C-terminal processing of a plant defense-related enzyme: primary structure of tobacco prepro-β-1.3-glucanase. Proc. Natl Acad Sci. USA 85, 5541-5545.
70. Sinnott, M. L. (1990). Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90, 1171-1202.
71. Somogyi, M. (1952). Notes on sugar determination. J. Biol. Chem. 195, 19-23.
72. Stark, M. J. R. and Boyd, A. (1986). The killer toxin of Kluyveromyces lactis: characterization of the toxin subunits and identification of the genes which encode them. EMBO J. 5, 1995-2002.
73. Struhl, K., Stinchcomb, D. T., Scherer, S. and Davis, R. W. (1979). High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules. Proc. Natl Acad. Sci. USA 76, 1035-1039.
74. Tanguy-Rougeau, C., Wésolowski-Louvel, M. and Fukuhara, H. (1988). The Kluyveromyces lactis KEXI gene encodes a subtilisin-type serine protease. FEBS Lett. 234, 464-470.
75. Tingle, M. A. and Halvorson, H. O. (1971). A comparison of β-glucanase and β-glucosidase in Saccharomyces lactis. Biochim. Biophys. Acta 250, 165-171.
76. van de Rhee, M. D., Mendes, O., Werten, M. W. T., Huizing, H. J. and Mooibroek, H. (1996). Highly efficient homologous integration via tandem exo-β-1,3-glucanase genes in the common mushroom. Agaricus bisporus. Curr. Genet. 30, 166-173.
77. Vazquez de Aldana, C. R., Correa, J., San Segundo, P., Bueno, A., Nebreda, A. R., Mendez, E. and Rey, F. del. (1991). Nucleotide sequence of the exo-1,3-β-glucanase encoding gene. EXG1, of the yeast Saccharomyces cerevisiae. Gene 97, 173-182.
78. Vieira, J. and Messing, J. (1987). Production of single-stranded plasmid DNA. Methods Enzymol. 153, 3-11.
79. Villa, T. G., Notario, V. and Villanueva, J. R. (1975). β-Glucanases of the yeast Pichia polymorpha. Arch. Microbiol. 104, 201-206.
80. Villa, T. G., Lachance, M. A. and Phaff, H. J. (1978). β-Glucanases of the yeast Kluyveromyces phaseolosporus: partial purification and characterization. Exp. Mycol. 2, 12-25.
81. von Heijne, G. (1983). Patterns of amino acids near signal-sequence cleavage sites. Eur. J. Biochem. 133, 17-21.
82. von Heijne, G. (1984). Analysis of the distribution of charged residues in the N-terminal region of signal sequences: implications for protein export in prokaryotic and eukaryotic cells. EMBO J. 3, 2315-2318.
83. Wang, Q., Tull, D., Meinke, A., Gilkes, N. R., Warren, R. A. J., Aebersold, R. and Withers, S. G. (1993). Glu280 is the nucleophile in the active site of Clostridium thermocellum Ce1C. a family A endo-β-1,4-glucanase. J. Biol. Chem. 268, 14,096-14,102.
84. Zaret, K. S. and Sherman, F. (1982). DNA sequence required for efficient transcription termination in yeast. Cell 28, 563-573.
85. Zvelebil, M. J. J. M. and Sternberg, M. J. E. (1988). Analysis and prediction of the location of catalytic residues in enzymes. Protein Eng. 2, 127-138. Yeast 15, 111-121 (1999)