Cerato-populin and cerato-platanin, two non-catalytic proteins from phytopathogenic fungi, interact with hydrophobic inanimate surfaces and leaves

Molecular Biotechnology

Volumn 55, Issue 1, 2013, Pages 27-42

  Martellini, Federica ^a   Faoro, Franco ^b   Carresi, Lara ^a   Pantera, Barbara ^a   Baccelli, Ivan ^a   Maffi, Dario ^b   Tiribilli, Bruno ^c   Sbrana, Francesca ^c   Luti, Simone ^a   Comparini, Cecilia ^a   Bernardi, Rodolfo ^d   Cappugi, Gianni ^a   Scala, Aniello ^a   Pazzagli, Luigia ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF PISA   (Italy)

Author keywords

Cloning; Defense responses; Expression; Hydrophobic surfaces; Leaf cuticle; PAMP; Protein aggregation; Protein characterization

Indexed keywords

DEFENSE RESPONSE; EXPRESSION; HYDROPHOBIC SURFACES; LEAF CUTICLE; PAMP; PROTEIN AGGREGATION; PROTEIN CHARACTERIZATION;

AGGREGATES; CLONING; HYDROPHOBICITY; MICA; SURFACE CHEMISTRY;

RECOMBINANT PROTEINS;

CERATO PLATANIN PROTEIN; CERATO POPULIN PROTEIN; FUNGAL PROTEIN; GOLD; MICA; POLITEF; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL DEATH; CIRCULAR DICHROISM; FLUORESCENCE SPECTROSCOPY; FUNGUS; HYDROPHOBICITY; IMMUNOGOLD LABELING; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PICHIA PASTORIS; PLANT LEAF; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

FUNGI;

EID: 84882452447     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-012-9618-4     Document Type: Article

References (57)

1. Templeton, M. D., Rikkerink, E. H. A., & Beever, R. E. (1994). Cysteine-rich proteins and recognition in fungal plant interactions. Molecular Plant-Microbe Interactions, 7, 320-325.
2. Stergiopoulos, I., & De Wit, P. J. (2009). Fungal effector proteins. Annual Review of Phytopathology, 47, 233-263.
3. Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323-329.
4. De Wit, J. G. M., Mehrabi, R., Van den Burg, H., & Stergiopoulos, I. (2009). Fungal effector proteins: Past, present and future. Molecular Plant Pathology, 10, 735-747.
5. Boller, T., & Felix, G. (2009). A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern recognition receptors. Annual Review of Plant Biology, 60, 379-406.
6. Zipfel, C. (2009). Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology, 12, 414-420.
7. Iriti, M., & Faoro, F. (2009). Chitosan as a MAMP, searching for a PRR. Plant Signaling & Behavior, 4, 66-68.
8. Almagro, L., Gómez Ros, L. V., Belchi-Navarro, S., Bru, R., Ros Barceló, A., & Pedreño, M. A. (2009). Class III peroxidases in plant defence reactions. Journal of Experimental Botany, 60(Suppl. 2), 377-390.
9. Pitzschke, A., Schikora, A., & Hirt, H. (2009). MAPK cascade signalling networks in plant defence. Current Opinion in Plant Biology, 12, 421-426.
10. Talbot, N. J. (1999). Fungal biology coming up for air and sporulation. Nature, 398, 295-296.
11. Sunde, M., Kwan, A. H., Templeton, M. D., Beever, R. E., & Mackay, J. P. (2008). Structural analysis of hydrophobins. Micron, 39, 773-784.
12. De Vocht, M. L., Reviakine, I., Ulrich, W. P., Bergsma-Schutter, W., Wösten, H. A., Vogel, H., et al. (2002). Self-assembly of the hydrophobin SC3 proceeds via two structural intermediates. Protein Science, 11, 1199-1205.
13. Kwan, A. H., Winefield, R. D., Sunde, M., Matthews, J. M., Haverkamp, R. G., Templeton, M. D., et al. (2006). Structural basis for rodlet assembly in fungal hydrophobins. Proceedings of the National Academy of Sciences of the United States of America, 103, 3621-3626.
14. Kim, S., Ahn, I. P., Rho, H. S., & Lee, Y. H. (2005). MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Molecular Microbiology, 57, 1224-1237.
15. Pazzagli, L., Pantera, B., Carresi, L., Zoppi, C., Pertinhez, T. A., Spisni, A., et al. (2006). Cerato-platanin, the first member of a new fungal protein family: Cloning, expression, and characterization. Cell Biochemistry and Biophysics, 44, 512-521.
16. Wilson, L. M., Idnurm, A., & Howlett, B. J. (2002). Characterization of a gene (sp1) encoding a secreted protein from Leptosphaeria maculans, the blackleg pathogen of Brassica napus. Molecular Plant Pathology, 3, 487-493.
17. Jeong, J. S., Mitchell, T. K., & Dean, R. A. (2007). The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence. FEMS Microbiology Letters, 273, 157-165.
18. Zaparoli, G., Cabrera, O. G., Medrano, F. J., Tiburcio, R., Lacerda, G., & Guimarães Pereira, G. (2009). Identification of a second family of genes in Moniliophthora perniciosa, the causal agent of witches broom disease in cacao, encoding necrosis-inducing proteins similar to cerato-platanins. Mycological Research, 113, 61-72.
19. Djonović, S., Vargas, W. A., Kolomiets, M. V., Horndeski, M., Wiest, A., & Kenerley, C. M. (2007). A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiology, 145, 875-889.
20. Vargas, W. A., Djonović, S., Sukno, S. A., & Kenerley, C. M. (2008). Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. Journal of Biological Chemistry, 283, 19804-19815.
21. Seidl, V., Marchetti, M., Schandl, R., Allmaier, G., & 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 Journal, 273, 4346-4359.
22. Yang, Y., Zhang, H., Li, G., Li, W., Wang, X., & Song, F. (2009). Ectopic expression of MgSM1, a cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnology Journal, 7, 763-777.
23. Frías, M., González, C., & Brito, N. (2011). BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytologist, 192(2), 483-495.
24. Pazzagli, L., Cappugi, G., Manao, G., Camici, G., Santini, A., & Scala, A. (1999). Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. Journal of Biological Chemistry, 274, 24959-24964.
25. Scala, A., Pazzagli, L., Comparini, C., Santini, A., Tegli, S., & Cappugi, G. (2004). Cerato-platanin an early-produced protein by Ceratocystis fimbriata f. sp. platani elicits phytoalexin synthesis in host and non-host plants. Journal of Plant Pathology, 86, 23-29.
26. Comparini, C., Carresi, L., Pagni, E., Sbrana, F., Sebastiani, F., Luchi, N., et al. (2009). New proteins orthologous to cerato-platanin in various Ceratocystis species and the purification and characterization of cerato-populin from Ceratocystis populicola. Applied Microbiology and Biotechnology, 84, 309-322.
27. Boddi, S., Comparini, C., Calamassi, R., Pazzagli, L., Cappugi, G., & Scala, A. (2004). Immunolocalization of cerato-platanin protein in cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani. FEMS Microbiology Letters, 233, 341-346.
28. Fontana, F., Santini, A., Salvini, M., Pazzagli, L., Cappugi, G., Scala, A., et al. (2008). Cerato-platanin pre-treated plane leaves restrict Ceratocystis platani growth and overexpress defense-related genes. Journal of Plant Phatolology, 90, 295-306.
29. Bernardi, R., Baccelli, I., Carresi, L., Comparini, C., Pazzagli, L., & Scala, A. (2010). Cerato-platanin elicits transcription of defence-related genes earlier than Ceratocystis platani on Platanus acerifolia. Forest Pathology,. doi: 10.1111/j.1439-0329.2010.00668.x.
30. Oliveira, A. L., Gallo, M., Pazzagli, L., Celso, E., Benedetti, C. E., Cappugi, G., et al. (2011). The structure of the elicitor cerato-platanin (cp), the first member of the cp fungal protein family, reveals a double ψ-barrel fold and carbohydrate binding. Journal of Biological Chemistry, 286, 17560-17568.
31. Sbrana, F., Bongini, L., Cappugi, G., Fanelli, D., Guarino, A., Pazzagli, L., et al. (2007). Atomic force microscopy images suggest aggregation mechanism in cerato-platanin. European Biophysics Journal, 36, 727-732.
32. Pazzagli, L., Zoppi, C., Carresi, L., Tiribilli, B., Sbrana, F., Schiff, S., et al. (2009). Characterization of ordered aggregates of cerato-platanin and their involvement in fungus-host interactions. Biochimica et Biophysica Acta, 1790, 1334-1344.
33. Kombrink, A. (2012). Heterologous production of fungal effectors in Pichia pastoris. Methods in Molecular Biology, 835, 209-217.
34. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: A laboratory manual (2nd ed.). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
35. Carresi, L., Pantera, B., Zoppi, C., Cappugi, G., Oliveira, A. L., Pertinhez, T. A., et al. (2006). Cerato-platanin, a phytotoxic protein from Ceratocystis fimbriata: Expression in Pichia pastoris, purification and characterization. Protein Expression Purification, 49, 159-167.
36. Benson, J. R., & Hare, P. E. (1975). O-phthalaldeyde: Fluorogenic detection of primary amines in the picomole range. Comparison with fluorescamine and ninhydrin. Proceedings of the National Academy of Sciences of the United States of America, 72, 619-622.
37. Roepstorff, P., Larsen, M. R., Rahbek-Nielsen, H., Nordhoff, E. (1998). Sample preparation for matrix assisted laser desorption/ionization mass spectrometry for peptides, protein and nucleic acid. Cell biology: A laboratory handbook (2nd ed.), Vol. 4. New York: Academic Press.
38. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
39. Le Vine, H. (1999). Quantification of the β-sheet amyloid fibril structures with Thioflavin T. Methods in Enzymology, 309, 274-284.
40. Duchet, J., Chabert, B., Chapel, J. P., Gerard, J. F., Chovelon, J. M., & Renault, N. J. (1997). Influence of the deposition process on the structure of grafted alkylsilane layers. Langmuir, 13, 2271-2278.
41. Xiao, Z., Xu, M., Sagisaka, K., & Fujita, D. (2003). AFM observations of self-assembled lambda DNA network on silanized mica. Thin Solid Films, 438, 114-117.
42. De Vocht, M. L., Scholtmeijer, K., van der Vegte, E. W., De Vries, O. M., Sonveaux, N., Wösten, H. A., et al. (1998). Structural characterization of the hydrophobin SC3, as a monomer and after self-assembly at hydrophobic/hydrophilic interfaces. Biophysical Journal, 74, 2059-2068.
43. El Modafar, C., Clérivet, A., Vigouroux, A., & Macheix, J. J. (1995). Accumulation of phytoalexins in leaves of plane tree (Platanus spp.) expressing susceptibility or resistance to Ceratocystis fimbriata f. sp. platani. European Journal of Plant Phatology, 101, 503-509.
44. Logemann, J., Schell, J., & Willmitzer, L. (1987). Improved method for the isolation of RNA from plant tissues. Anaytical Biochemistry, 163, 16-20.
45. Faoro, F., Tornaghi, R., & Belli, G. (1991). Localization of the closteroviruses on grapevine thin-section and their identification by immunogold labelling. Journal of Phytopathology: Phytopathologische Zeitschrift, 133, 297-306.
46. Van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology, 44, 135-162.
47. Chiti, F., & Dobson, C. M. (2006). Protein misfolding, functional amyloid, and human disease. Annual Review Biochemistry, 75, 333-366.
48. Lomakin, A., Chung, D. S., Benedek, G. B., Kirschner, D. A., & Teplow, D. B. (1996). On the nucleation and growth of amyloid beta-protein fibrils: Detection of nuclei and quantitation of rate constants. Proceedings of the National Academy of Sciences of the United States of America, 93, 1125-1129.
49. Bellotti, V., & Chiti, F. (2008). Amyloidogenesis in its biological environment: Challenging a fundamental issue in protein misfolding diseases. Current Opinion in Structural Biology, 18, 771-779.
50. Wösten, H. A. B., Richter, M., & Willey, J. M. (1999). Structural proteins involved in emergence of microbial aerial hyphae. Fungal Genetics and Biology, 27, 153-160.
51. Fowler, D. M., Koulov, A. V., Balch, W. E., & Kelly, J. K. (2007). Functional amyloid - from bacteria to humans. Trends Biochemical Sciences, 32, 217-224.
52. Epstein, E. A., & Chapman, M. R. (2008). Polymerizing the fibre between bacteria and host cells: The biogenesis of functional amyloid fibres. Cellular Microbiology, 10, 1413-1420.
53. Hammerschmidt, R. (1999). Phytoalexins: What we have learned after 60 years? Annual Review of Phytopathology, 37, 285-306.
54. Bessire, M., Chassot, C., Jacquat, A. C., Humphry, M., Borel, S., Jean MacDonald Petetot-Comber, J., et al. (2007). Permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. The EMBO Journal, 26, 2158-2168.
55. Chassot, C., Nawrath, C., & Métraux, J. P. (2008). The cuticle: Not only a barrier for plant defence. Plant Signaling & Behavior, 3(Suppl 2), 142-144.
56. Reina-Pinto, J. J., & Yephremov, A. (2009). Surface lipids and plant defenses. Plant Physiology and Biochemistry, 47, 540-549.
57. Chassot, C., Nawrath, C., & Métraux, J. P. (2007). Cuticular defects lead to full immunity to a major plant pathogen. Plant Journal, 49, 972-980.