Biocontrol activity of an alkaline serine protease from Aureobasidium pullulans expressed in Pichia pastoris against four postharvest pathogens on apple

International Journal of Food Microbiology

Volumn 182-183, Issue , 2014, Pages 1-8

  Banani, Houda ^a   Spadaro, Davide ^a   Zhang, Dianpeng ^a,b   Matic, Slavica ^a   Garibaldi, Angelo ^a   Gullino, Maria Lodovica ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

Author keywords

Alternaria alternata; Botrytis cinerea; Monilinia fructicola; Penicillium expansum; Postharvest; Recombinant expression

Indexed keywords

ESCHERICHIA COLI PROTEIN; SERINE PROTEINASE;

ALTERNARIA ALTERNATA; ANTIFUNGAL ACTIVITY; APPLE; ARTICLE; AUREOBASIDIUM PULLULANS; BIOLOGICAL PEST CONTROL; BOTRYTIS CINEREA; CELL WALL; ENZYME ACTIVITY; FUNGUS; IN VITRO STUDY; IN VIVO STUDY; MICROSCOPY; MONILINIA FRUCTICOLA; NONHUMAN; NUCLEOTIDE SEQUENCE; PENICILLIUM EXPANSUM; PICHIA PASTORIS; POSTHARVEST PERIOD; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SPORE GERMINATION;

ALTERNARIA ALTERNATA; BOTRYTIS CINEREA; MONILINIA FRUCTICOLA; PENICILLIUM EXPANSUM; POSTHARVEST; RECOMBINANT EXPRESSION;

ANTIFUNGAL AGENTS; ASCOMYCOTA; FOOD HANDLING; FOOD MICROBIOLOGY; HYPHAE; MALUS; MITOSPORIC FUNGI; PEST CONTROL, BIOLOGICAL; PICHIA; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; SPORES, FUNGAL;

EID: 84901029928     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.05.001     Document Type: Article

References (54)

1. Balamurugan V., Reddy G.R., Suryanarayana V.V.S. Pichia pastoris: a notable heterologous expression system for the production of foreign proteins-vaccines. Indian J. Biotechnol. 2007, 6:175-186.
2. Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 1968, 22:87-108.
3. Bencheqroun S.K., Bajji M., Massart S., Labhilili M., El-Jafari S., Jijakli M.H. In vitro and in situ study of postharvest apple blue mold biocontrol by Aureobasidium pullulans: evidence for the involvement of competition for nutrients. Postharvest Biol. Technol. 2007, 46:128-135.
4. Bolignano G., Criseo G. Disseminated nosocomial fungal infection by Aureobasidium pullulans var. melanigenum: a case report. J. Clin. Microbiol. 2003, 41:4483-4485.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:1105-1112.
6. Cantu D., Greve C., Labavitch J.M., Powell A.L.T. Characterization of the cell wall of the ubiquitous plant pathogen Botrytis cinerea. Mycol. Res. 2009, 113:1396-1403.
7. Cregg J.M., Vedvick T.S., Raschke W.C. Recent advances in the expression of foreign genes in Pichia pastoris. Biotechnology 1993, 11:905-910.
8. De Groot P.W.J., Ram A.F., Klis F.M. Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet. Biol. 2005, 42:657-675.
9. De Oliveira L.R., Moraes-Souza H., Maltos A.L., Santos K.C., Molina R.J., Barata C.H. Aureobasidium pullulans infection in a patient with chronic lymphocytic leukemia. Rev. Soc. Bras. Med. Trop. 2013, 46:660-662.
10. Droby S., Wisniewski M., Macarisin D., Wilson C. Twenty years of postharvest biocontrol research: is it time for a new paradigm?. Postharvest Biol. Technol. 2009, 52:137-145.
11. EFSA Potential inclusion of the microorganism Aureobasidium pullulans strains DSM 14940 and DSM 14941 in Annex IV of Regulation (EC) No 396/2005. EFSA J. 2011, 9(11):2435.
12. Feijoo-Siota L., Villa T. Native and biotechnologically engineered plant proteases with industrial applications. Food Bioproc. Technol. 2011, 4:1066-1088.
13. Gonzalez V., Tello M.L. The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers. 2011, 47:29-42.
14. Gupta R., Beg O.K., Lorenz P. Bacterial alkaline proteases: molecular approaches and industrial applications. Appl. Microbiol. Biotechnol. 2002, 59:15-32.
15. Hawkes M., Rennie R., Sand C., Vaudry W. Aureobasidium pullulans infection: fungemia in an infant and a review of human cases. Diagn. Microbiol. Infect. Dis. 2005, 51:209-213.
16. Holmes G.J., Eckert J.W. Sensitivity of Penicillium digitatum and P. italicum to postharvest citrus fungicides in California. Phytopathology 1999, 89:716-721.
17. Huang Y.T., Liaw S.J., Liao C.H., Yang J.L., Lai D.M., Lee Y.C., Hsueh P.R. Catheter-related septicemia due to Aureobasidium pullulans. Int. J. Infect. Dis. 2008, 12:137-139.
18. Inamura H., Nakai T., Muroga K. An extracellular protease produced by Vibrio anguillarum. Bull. Jpn. Soc. Sci. Fish. 1985, 51:1915-1920.
19. Ippolito A., Ghaouth A.E., Wilson C.L., Wisniewski M. Control of postharvest decay of apple fruit by Aureobasidium pullulans and induction of defense responses. Postharvest Biol. Technol. 2000, 19:265-272.
20. Jamalizadeh M., Etebarian H.R., Aminian H., Alizadeh A. A review of mechanisms of action of biological control organisms against post-harvest fruit spoilage. EPPO Bull. 2011, 41:65-71.
21. Janisiewicz W.J., Korsten L. Biological control of postharvest diseases of fruits. Annu. Rev. Phytopathol. 2002, 40:411-441.
22. Janisiewicz W.J., Kurtzman C.P., Buyer J.S. Yeasts associated with nectarines and their potential for biological control of brown rot. Yeast 2010, 27:389-398.
23. Kader A.A. Postharvest Technology of Horticultural Crops 2002, UCANR Publications, California.
24. Kawamura C., Tsujimoto T., Tsuge T. Targeted disruption of a melanin biosynthesis gene affects conidial development and UV tolerance in the Japanese pear pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 1999, 12:59-63.
25. Khamis Y., Ligorio A., Sanzani S.M., Nigro F., Ippolito A. Control of storage diseases of citrus by pre- and postharvest application of salts. Postharvest Biol. Technol. 2012, 72:57-63.
26. Kishore K.H., Kanjilal S., Misra S., Reddy C.R., Murty U.S. Comparative chemical characterization of pigmented and less pigmented cell walls of Alternaria tenuissima. Curr. Microbiol. 2005, 51:399-401.
27. Klis F.M., Mol P., Hellingwerf K., Brul S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2002, 26:239-256.
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
29. Lima G., Ippolito A., Nigro F., Salerno M. Effectiveness of Aureobasidium pullulans and Candida oleophila against postharvest strawberry rots. Postharvest Biol. Technol. 1997, 10:169-178.
30. Lopez-Reyes J.G., Spadaro D., Garibaldi A., Gullino M.L. Efficacy of plant essential oils on postharvest control of rot caused by fungi on four cultivars of apples in vivo. Flavour Fragr. J. 2010, 25:171-177.
31. Macauley-Patrick S., Fazenda M.L., McNeil B., Harvey L.M. Heterologous protein production using the Pichia pastoris expression system. Yeast 2005, 22:249-270.
32. Macchione M.M., Merheb C.W., Eleni Gomes E., Silva R. Protease production by different thermophilic fungi. Appl. Biochem. Biotechnol. 2008, 146:223-230.
33. Martini C., Spadoni A., Mari M. First report of brown rot caused by Monilinia fructicola on apple in Italy. Plant Dis. 2013, 97:689.
34. Morton C.L., Potter P.M. Comparison of Escherichia coli, Saccharomyces cerevisiae, Pichia pastoris, Spodoptera frugiperda, and COS7 cells for recombinant gene expression: application to a rabbit liver carboxylesterase. Mol. Biotechnol. 2000, 16:193-202.
35. Nunes C. Biological control of postharvest diseases of fruit. Eur. J. Plant Pathol. 2012, 133:181-196.
36. Pellegrino C., Gullino M.L., Garibaldi A., Spadaro D. First report of brown rot of stone fruit caused by Monilinia fructicola in Italy. Plant Dis. 2009, 93:668.
37. Pessoni R.A.B., Freshour G., Figueiredo-Ribeiro R.C.L., Hahn M.G., Braga M.R. Cell-wall structure and composition of Penicillium janczewskii as affected by inulin. Mycologia 2005, 97:304-311.
38. Saravanakumar D., Ciavorella A., Spadaro D., Garibaldi A., Gullino M.L. Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata and Penicillium expansum in apples through iron depletion. Postharvest Biol. Technol. 2008, 49:121-128.
39. Saravanakumar D., Spadaro D., Garibaldi A., Gullino M.L. Detection of enzymatic activity and partial sequence of a chitinase gene in Metschnikowia pulcherrima strain MACH1 used as post-harvest biocontrol agent used as post-harvest biocontrol agent. Eur. J. Plant Pathol. 2009, 123:183-193.
40. Schallmey M., Singh A., Ward O.P. Developments in the use of Bacillus species in industrial production. Can. J. Microbiol. 2004, 50:1-17.
41. Schena L., Nigro F., Pentimone I., Ligorio A., Ippolito A. Control of postharvest rots of sweet cherries and table grapes with endophytic isolates of Aureobasidium pullulans. Postharvest Biol. Technol. 2003, 30:209-220.
42. Schlumbaum A., Mauch F., Vogeli U., Boller T. Plant chitinases are potent inhibitors of fungal growth. Nature 1986, 324:365-367.
43. Singh D., Sharma R.R. Postharvest diseases of fruit and vegetables and their management. Sustainable Pest Management 2007, 321-334. Daya Publishing House, New Delhi. D. Prasad (Ed.).
44. Snowdon A.L. A Color Atlas of Post-harvest Diseases and Disorders of Fruits and Vegetables: General Introduction and Fruits 1990, vol. 1. CRC Press, Boca Raton.
45. Spadaro D., Sabetta W., Acquadro A., Portis E., Garibaldi A., Gullino M.L. Use of AFLP for differentiation of Metschnikowia pulcherrima strains for postharvest disease biological control. Microbiol. Res. 2008, 163:523-530.
46. Wang H., Li J., Bostock R.M., Glichrist D.G. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 1996, 8:375-391.
47. Wessels J.G.H. Cell wall synthesis in apical hyphal growth. Int. Rev. Cytol. 1986, 104:37-79.
48. Yan R., Ding D., Guan W., Hou J., Li M. Control of grey mould rot of loquat with chitinase expressed in Pichia pastoris. Crop. Prot. 2008, 27:1312-1317.
49. Yang H., Liu L., Shin H.D., Chen R.R., Li J., Du G., Chen J. Comparative analysis of heterologous expression, biochemical characterization optimal production of an alkaline a-amylase from alkaliphilic Alkalimonas amylolytica in Escherichia coli and Pichia pastoris. Biotechnol. Prog. 2012, 29:39-47.
50. Zhang D., Spadaro D., Garibaldi A., Gullino M.L. Selection and evaluation of new antagonists for their efficacy against postharvest brown rot of peaches. Postharvest Biol. Technol. 2010, 55:174-181.
51. Zhang D., Spadaro D., Garibaldi A., Gullino M.L. Efficacy of the antagonist Aureobasidium pullulans PL5 against postharvest pathogens of peach, apple and plum and its modes of action. Biol. Control 2010, 54:172-180.
52. Zhang D., Spadaro D., Garibaldi A., Gullino M.L. Potential biocontrol activity of a strain of Pichia guilliermondii against grey mould of apples and its possible modes of action. Biol. Control 2011, 57:193-201.
53. Zhang D., Spadaro D., Valente S., Garibaldi A., Gullino M.L. Cloning, characterization, expression and antifungal activity of an alkaline serine protease of Aureobasidium pullulans PL5 involved in the biological control of postharvest pathogens. Int. J. Food Microbiol. 2012, 153:453-464.
54. Zhu S.J. Non-chemical approaches to decay control in postharvest fruit. Advances in Postharvest Technologies for Horticultural Crops 2006, 297-313. Research Signpost, Trivandrum. B. Noureddine, S. Norio (Eds.).