Self-assembly at air/water interfaces and carbohydrate binding properties of the small secreted protein EPL1 from the fungus Trichoderma atroviride

Journal of Biological Chemistry

Volumn 288, Issue 6, 2013, Pages 4278-4287

  Frischmann, Alexa ^a   Neudl, Susanna ^c   Gaderer, Romana ^a   Bonazza, Klaus ^a   Zach, Simone ^a   Gruber, Sabine ^a   Spadiut, Oliver ^b   Friedbacher, Gemot ^a   Grothe, Hinrich ^c   Seidl Seiboth, Verena ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^b Institute of Biochemical Engineering   (Austria)

^c VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AIR/WATER INTERFACES; ALLERGIC REACTIONS; AMPHIPHILICS; ATOMIC FORCE; BIOCHEMICAL PROPERTIES; BIOLOGICAL PROCESS; CARBOHYDRATE BINDING; DEFENSE RESPONSE; FILAMENTOUS FUNGI; FUNGAL GROWTH; GROWTH CONDITIONS; HYDROPHOBINS; HYPHAL GROWTH; KNOCK OUTS; PRIMARY FUNCTIONS; PROTEIN FAMILY; PROTEIN LAYERS; SECRETED PROTEIN; SPORE FORMATION; SURFACE ACTIVITIES; TRICHODERMA ATROVIRIDE;

ATOMIC FORCE MICROSCOPY; BINDING ENERGY; CARBOHYDRATES; FUNGI; GENE EXPRESSION;

PROTEINS;

CARBOHYDRATE; FUNGAL PROTEIN; HYDROPHOBIN; SMALL SECRETED PROTEIN EPL1; UNCLASSIFIED DRUG; WATER;

AIR; AQUEOUS SOLUTION; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL POLARITY; CELL SURFACE; CONTROLLED STUDY; EPL GENE; EPL1 GENE; EPL2 GENE; EPL3 GENE; FUNGAL GENOME; FUNGAL STRAIN; FUNGUS; FUNGUS GROWTH; FUNGUS HYPHAE; GENE EXPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN STRUCTURE; SPOROGENESIS; TRICHODERMA ATROVIRIDE;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKDOWN TECHNIQUES; GENOME, FUNGAL; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; TRICHODERMA;

EID: 84873665639     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.427633     Document Type: Article

References (34)

1. Kubicek, C. P., Herrera-Estrella, A., Seidl-Seiboth, V., Martinez, D. A., Druzhinina, I. S., Thon, M., Zeilinger, S., Casas-Flores, S., Horwitz, B. A., Mukherjee, P. K., Mukherjee, M., Kredics, L., Alcaraz, L. D., Aerts, A., Antal, Z., Atanasova, L., Cervantes-Badillo, M. G., Challacombe, J., Chert-kov, O., McCluskey, K., Coulpier, F., Deshpande, N., von Döhren, H., Ebbole, D. J., Esquivel-Naranjo, E. U., Fekete, E., Flipphi, M., Glaser, F., Gómez-Rodríguez, E. Y., Gruber, S., Han, C., Henrissat, B., Hermosa, R., Hernández-Oñate, M., Karaffa, L., Kosti, I., Le Crom, S., Lindquist, E., Lucas, S., Lübeck, M., Lübeck, P. S., Margeot, A., Metz, B., Misra, M., Nevalainen, H., Omann, M., Packer, N., Perrone, G., Uresti-Rivera, E. E., Salamov, A., Schmoll, M., Seiboth, B., Shapiro, H., Sukno, S., Tamayo-Ramos, J. A., Tisch, D., Wiest, A., Wilkinson, H. H., Zhang, M., Coutinho, P. M., Kenerley, C. M., Monte, E., Baker, S. E., and Grigoriev, I. V. (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12, R40
2. Martin, F., Aerts, A., Ahrén, D., Brun, A., Danchin, E. G., Duchaussoy, F., Gibon, J., Kohler, A., Lindquist, E., Pereda, V., Salamov, A., Shapiro, H. J., Wuyts, J., Blaudez, D., Buée, M., Brokstein, P., Canbäck, B., Cohen, D., Courty, P. E., Coutinho, P. M., Delaruelle, C., Detter, J. C., Deveau, A., DiFazio, S., Duplessis, S., Fraissinet-Tachet, L., Lucic, E., Frey-Klett, P., Fourrey, C., Feussner, I., Gay, G., Grimwood, J., Hoegger, P. J., Jain, P., Kilaru, S., Labbé, J., Lin, Y. C., Legué, V., Le Tacon, F., Marmeisse, R., Melayah, D., Montanini, B., Muratet, M., Nehls, U., Niculita-Hirzel, H., Oudot-Le Secq, M.P., Peter, M., Quesneville, H., Rajashekar, B., Reich, M., Rouhier, N., Schmutz, J., Yin, T., Chalot, M., Henrissat, B., Kües, U., Lucas, S., Van de Peer, Y., Podila, G. K., Polle, A., Pukkila, P. J., Richardson, P. M., Rouzé, P., Sanders, I.R., Stajich, J.E., Tunlid, A., Tuskan, G., and Grigoriev, I. V. (2008) The genome of Laccaria bicolor provides insights into mycor-rhizal symbiosis. Nature 452, 88-92
3. Pazzagli, L., Cappugi, G., Manao, G., Camici, G., Santini, A., and Scala, A. (1999) Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. pla-tani. J. Biol. Chem. 274, 24959-24964
4. Cole, G. T., Zhu, S. W., Pan, S. C., Yuan, L., Kruse, D., and Sun, S. H. (1989) Isolation of antigens with proteolytic activity from Coccidioides immitis. Infect. Immun. 57, 1524-1534
5. Kurup, V.P., Banerjee, B., Hemmann, S., Greenberger, P. A., Blaser, K., and Crameri, R. (2000) Selected recombinant Aspergillus fumigatus allergens bind specifically to IgE in ABPA. Clin. Exp. Allergy 30, 988-993
6. Pan, S., and Cole, G. T. (1995) Molecular and biochemical characterization of a Coccidioides immitis-specific antigen. Infect. Immun. 63, 3994-4002
7. Scala, A., Pazzagli, L., Comparini, C., Santini, A., Tegli, S., and Cappugi, G. (2004) Cerato-platanin, an early-produced protein by Ceratocystis fim-briata f.sp. platani, elicits phytoalexin synthesis in host and non-host plants. J. Plant Pathol. 86, 27-33
8. Sharen, A. L., and Krupinski, G. (1970) Cultural and inoculation studies of Septoria nodorum, cause of Glume Blotch of wheat. Phytopathology 60, 1480-1485
9. Wilson, L. M., Idnurm, A., and Howlett, B. J. (2002) Characterization of a gene (sp1) encoding a secreted protein fromLeptosphaeria maculans, the blackleg pathogen of Brassica napus. Mol. Plant Pathol. 3, 487-493
10. Yang, Y., Zhang, H., Li, G., Li, W., Wang, X., and Song, F. (2009) Ectopic expression of MgSM1, a cerato-platanin family protein from Magna-porthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnol. J. 7, 763-777
11. Djonovic, S., Pozo, M. J., Dangott, L. J., Howell, C. R., and Kenerley, C. M. (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol. Plant Microbe Interact. 19, 838-853
12. Djonovic, S., Vargas, W. A., Kolomiets, M. V., Horndeski, M., Wiest, A., and Kenerley, C. M. (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145, 875-889
13. Vargas, W. A., Djonovic, S., Sukno, S. A., and Kenerley, C. M. (2008) Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. J. Biol. Chem. 283, 19804-19815
14. Seidl, V., Marchetti, M., Schandl, R., Allmaier, G., and Kubicek, C. P. (2006) Epl1, the major secreted protein of Hypocrea atroviridis on glucose, is a member of a strongly conserved protein family comprising plant defense response elicitors. FEBS J. 273, 4346-4359
15. Baccelli, I., Comparini, C., Bettini, P. P., Martellini, F., Ruocco, M., Pazza-gli, L., Bernardi, R., and Scala, A. (2012) The expression of the cerato-platanin gene is related to hyphal growth and chlamydospores formation in Ceratocystisplatani. FEMSMicrobiol. Lett. 327, 155-163
16. Boddi, S., Comparini, C, Calamassi, R., Pazzagli, L., Cappugi, G., and Scala, A. (2004) Cerato-platanin protein is located in the cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani. FEMS Microbiol. Lett. 233, 341-346
17. Limón, M. C, Chacón, M. R., Mejías, R., Delgado-Jarana, J., Rincón, A. M., Codón, A. C, and Benítez, T. (2004) Increased antifungal and chitinase specific activities of Trichoderma harzianum CECT 2413 by addition of a cellulose binding domain. Appl. Microbiol. Biotechnol. 64, 675-685
18. Wösten, H. A. (2001) Hydrophobins: multipurpose proteins. Annu. Rev. Microbiol. 55, 625-646
19. de Oliveira, A. L., Gallo, M., Pazzagli, L., Benedetti, C E., Cappugi, G., Scala, A., Pantera, B., Spisni, A., Pertinhez, T. A., and Cicero, D. O. (2011) The structure of the elicitor cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double i///3-barrel fold and carbohydrate binding. J. Biol. Chem. 286, 17560-17568
20. Sambrook, J., and Russell, D. W. (2001) Molecular Cloning: a Laboratory Manual, 2 Ed., pp. 7.1-7.74 and A.8.40-A.8.51, Cold Spring Harbor Laboratory Press, Plainview, NY
21. Shang, J., Flury, M., Harsh, J. B., and Zollars, R. L. (2010) Contact angles of aluminosilicate clays as affected by relative humidity and exchangeable cations. Colloids Surf. A Physicochem. Eng. Asp. 353, 1-9
22. Yang, D., Xu, Z., Liu, C, and Wang, L. (2010) Experimental study on the surface characteristics of polymer melts. Colloids Surf. A Physicochem. Eng Asp. 367, 174-180
23. Owens, D. K., and Wendt, R. C. (1969) Estimation of the surface free energy of polymers. J. Appl. Polym. Sci. 13, 1741-1747
24. Seidl, V., Huemer, B., Seiboth, B., and Kubicek, C. P. (2005) A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J. 272, 5923-5939
25. Wessel, D., and Flügge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
26. Seidl, V., Seiboth, B., Karaffa, L., and Kubicek, C. P. (2004) The fungal STRE-element-binding protein Seb1 is involved but not essential for glycerol dehydrogenase (gld1) gene expression and glycerol accumulation in Trichoderma atroviride during osmotic stress. Fungal Genet. Biol. 41, 1132-1140
27. Gruber, S., Vaaje-Kolstad, G., Matarese, F., López- Mondéjar, R., Kubicek, C. P., and Seidl-Seiboth, V. (2011) Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride. Glycobiology 21, 122-133
28. Penttilä, M., Nevalainen, H., Rättö, M., Salminen, E., and Knowles, J. (1987) A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61, 155-164
29. Mach, R. L., Schindler, M., and Kubicek, C. P. (1994) Transformation of Trichoderma reesei based on hygromycin B resistance using homologous expression signals. Curr. Genet. 25, 567-570
30. Catalano, V., Vergara, M., Hauzenberger, J. R., Seiboth, B., Sarrocco, S., Vannacci, G., Kubicek, C. P., and Seidl-Seiboth, V. (2011) Use of a nonhomologous end-joining-deficient strain (Aku70) of the biocontrol fungus Trichoderma virens to investigate the function of the laccase gene lcc1 in sclerotia degradation. Curr. Genet. 57, 13-23
31. López-Mondéjar, R., Catalano, V., Kubicek, C. P., and Seidl, V. (2009) The β-N-acetylglucosaminidases NAG1 andNAG2 are essential for growth of Trichoderma atroviride on chitin. FEBSJ. 276, 5137-5148
32. Askolin, S., Penttilä, M., Wösten, H. A., and Nakari-Setälä, T. (2005) The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol. Lett. 253, 281-288
33. Ruiz-Herrera, J. (1991) Fungal Cell Wall: Structure, Synthesis and Assembly, p. 92, CRC Press, Boca Raton, FL
34. Cosgrove, D. J. (2000) Loosening of plant cell walls by expansins. Nature 407, 321-326