Ability of moderately halophilic bacteria to control grey mould disease on tomato fruits

Journal of Phytopathology

Volumn 156, Issue 1, 2008, Pages 42-52

  Sadfi Zouaoui, N ^a,b   Essghaier, B ^a,b   Hajlaoui, M R ^a,c   Fardeau, M L ^a,d   Cayaol, J L ^a,d   Ollivier, B ^a,d   Boudabous, A ^a,b  

^a UNIVERSITY OF TUNIS   (Tunisia)

^b FACULTÉ DES SCIENCES DE TUNIS   (Tunisia)

^c UNIVERSITY OF CARTHAGE   (Tunisia)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Bacterial characterization; Biocontrol; Botrytis cinerea; Grey mould; Halophilic bacteria; Hydrolytic enzymes; Postharvest diseases; Tomatoes

Indexed keywords

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOCONTROL AGENT; COMPARATIVE STUDY; ENZYME; FRUIT; FUNGAL DISEASE; FUNGUS; SALINITY TOLERANCE; VEGETABLE;

AFRICA; NORTH AFRICA; TUNISIA;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; BOTRYTIS; HALOBACILLUS HALOPHILUS; HALOBACILLUS LITORALIS; HALOBACILLUS TRUEPERI; HALOMONAS; HALOMONAS SUBGLACIESCOLA; HALOMONAS VARIABILIS; LYCOPERSICON ESCULENTUM; MARINOCOCCUS HALOPHILUS; PLANOCOCCUS RIFIETOENSIS; SALINICOCCUS ROSEUS;

EID: 37249020186     PISSN: 09311785     EISSN: 14390434     Source Type: Journal    
DOI: 10.1111/j.1439-0434.2007.01329.x     Document Type: Article

References (80)

1. Barritt MM 1936) The intensification of the Voges-Proskauer reaction by the addition of α-naphtol. J Pathol Bacteriol 42 : 441 445.
2. Benhamou N, Chet I 1996) Parasitism of sclerotia of Sclerotium rolfsii by Trichoderma harzianum: ultrastructural and cytochemical aspects of the interaction. Phytopathology 86 : 405 416.
3. Benson D, Boguski MS, Lipman DJ, Ostell J, Ouellette BF, Rapp BA, Wheeler DL. (1999) GenBank. Nucleic Acids Res 27 : 12 17.
4. Chérif M, Benhamou N 1990) Cytochemical aspects of chitin breakdown during the parasitic action of a Trichoderma sp. on Fusarium oxysporum f.sp. radicis lycopersici. Phytopathology 80 : 1406 1414.
5. Chérif M, Sadfi N, Benhamou N, Boudabous A, Hajlaoui MR, Tirilly Y 2002) Ultrastructural and cytochemical aspects of the interaction of the antagonistic bacteria Bacillus cereus X16 and Bacillus thuringiensis 55T with Fusarium roseum var. sambucinum in vitro. J Plant Pathol 84 : 83 93.
6. Chernin L, Ismailov Z, Haran S, Chet I 1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ Microbiol 61 : 1720 1726.
7. Chigaleichik AG 1976) Chitinase of Bacillus thuringiensis. Mikrobiologiya 45 : 966 972.
8. Christensen WB 1946) Urea decomposition as a means of differentiating Proteus and paracolon cultures from each other and from Salmonella and Shigella. J Bacteriol 52 : 461 466.
9. Clarke PH 1953) Hydrogen sulphide production by bacteria. J Gen Microbiol 8 : 397 407.
10. Cook RJ, Baker KF. The Nature and Practice of Biological Control of Plant Pathogens. St Paul, MN, USA, APS Press, 1983, 539 pp.
11. Cowan DA. Industrial enzymes. In : Moses V, Cape RE (eds Biotechnology, the Science and the Business, Reading, UK, Harwood Academic Publishers, 1991, pp. 311 340.
12. Edwards SG. Biological Control of Botrytis cinerea by Bacillus brevis on Protected Chinese Cabbage. Aberdeen, UK, University of Aberdeen, 1993 (PhD thesis).
13. Elad Y, Zimand G. Intergration of biological and chemical control for grey mould. In : Verhoff K, Malathrakis NE, Williamson B (eds Recent Advances in Botrytis Research, Wageningen, the Netherlands, Pudoc, 1992, pp. 272 276.
14. Elad Y, Yunis H, Katan T 1992) Multiple resistance to benzimidazoles, dicarboximides and diethofencarb in field isolates of Botrytis cinerea in Israel. Plant Pathol 41 : 41 46.
15. Elad Y, Kohl J, Fokkeman N 1994) Control of infection and sporulation of Botrytis cinerea on bean and tomato by saprophytic bacteria and fungi. Eur J Plant Pathol 100 : 315 336.
16. Elad Y, Gullino ML, Shtienberg D, Aloi C 1995) Managing Botrytis cinerea on tomatoes in greenhouses in the Mediterranean. Crop Prot 14 : 105 109.
17. El-Ghaouth A, Charles LW, Wisniewski M 1998) Ultrastructural and cytochemical aspects of the biological control of Botrytis cinerea by Candidate sanitoana in apple fruit. Phytopathology 88 : 282 291.
18. Felsenstein J 1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 : 783 791.
19. Fiddman PJ, Rossall S 1995) Selection of bacterial antagonists for the biological control of Rhizocotonia solani in oilseed rape (Brassica napus). Plant Pathol 44 : 695 703.
20. Fox GE, Wisotzkey JD, Jurtshuk P 1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Evol Microbiol 42 : 166 170.
21. Frändberg E, Schnürer J 1994) Chitinolytic properties of Bacillus pabuli K1. J App Bacteriol 76 : 361 367.
22. Frasier WC 1926) A method for detection of changes in gelatin due to bacteria. J Infect Dis 39 : 302 309.
23. Fravel DR 1988) Role of antibiosis in the biocontrol of plant diseases. Ann Rev Phytopathol 26 : 75 91.
24. Grant WD, Kamekura M, Genity Mc, Ventosa A Family 1. In : Boone DR, Castenholz RW, Garrity GM (eds Bergey's Manual of Systematic Bacteriology, 2nd edn, Vol. 1, New York, NY, USA, Springer, 2001, pp. 299 339.
25. Hacene H, Rafa F, Chebhouni N, Boutaiba S, Bhatnagar T, Baratti JC, Ollivier B 2004) Biodiversity of prokaryotic microflora in El Golea Salt lake Algerian Sahara. J Arid Environ 58 : 273 284.
26. Hall TA 1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41 : 95 98.
27. Hmouni A, Hajlaoui MR, Mlaiki A 1996) Résistance de Botrytis cinerea aux benzimidazoles et aux dicarboximides dans les cultures abritées de tomate en Tunisie. Bull OEPP 26 : 697 705.
28. Hobson GE 1981) the short-term storage of tomato fruits. J Hortic Sci 56 : 363 368.
29. Jeffries CD, Holtman DF, Guse DG 1957) A rapid method for determining the activity of microorganisms on nucleic acids. J Bacteriol 73 : 591 613.
30. Jukes TH, Cantor CR. Evolution of protein molecules. In : Munro HN (ed. Mammalian Protein Metabolism, New York, NY, USA, Academic Press, 1969, pp. 211 232.
31. Kehlenbeck H, Krone C, Oerke EC, Schönbeck F 1994) the effectiveness of induced resistance on yield of mildewed barley. J Plant Dis Prot 101 : 11 21.
32. Kim DS, Cook RJ, Weller DM 1997) Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. Phytopathology 87 : 551 558.
33. Korsten L, De Jager ES, De Villiers EE, Lourens A, Wehner FC 1995) Evaluation of bacterial epiphytes isolated from avocado leaf and fruit surfaces for biocontrol of avocado postharvest diseases. Plant Dis 79 : 1149 1156.
34. Kovacs N 1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178 : 703 704.
35. Kulkarni N, Shendey A, Rao M 1999) Molecular and biotechnological aspects of xylanases. FEMS Mircobiol Rev 23 : 411 456
36. Kushner DJ. Life in high salt and solute concentrations: halophilic bacteria. In : Kushner DJ (ed. Microbial Life in Extreme Environments. London, UK, Academic Press, 1978, pp. 371 368.
37. Leelasuphakul W, Sivanunsakul P, Phongpaichit S 2006) Purification, characterization and synergetic activity of β-1, 3-glucanase and antibiotic extract from an antagonistic Bacillus subtilis NRS 89-24 against rice blast and sheath blight. Enzyme Microbial Technol 38 : 990 997.
38. Lim H, Kim Y, Kim S 1991) Pseudomonas stutzeri YLP-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl Environ Microbiol 57 : 510 516.
39. Locke T, Fletcher JT 1988) Incidence of Benomyl and iprodione resistance in isolates of Botrytis cinerea in tomato crops in England and Wales in 1986. Plant Pathol 37 : 381 384.
40. Lorito M, Di Pietro A, Hayes CK, Woo SL, Harman GE 1993) Antifungal, synergistic interaction between chitinolytic enzymes from Trichoderma harzianum and Enterobacter cloacae. Phytopathology 83 : 721 728.
41. Lowe GH 1962) the rapid detection of lactose fermentation in paracolon organisms by the demonstration of β-D-galactosidase. J Med Lab Technol 19 : 21.
42. Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM 2001) The RDP-II (Ribosomal Database project). Nucleic Acids Res 29 : 173 174.
43. Marangoni AG, Stanley DW 1991) Studies on the long-term storage of mature, green tomato fruit. J Hortic Sci 66 : 81 84
44. Mari M., Guizzardi M, Brunelli M, Folchi A 1996) Postharvest biological control of grey mould (Botrytis cinerea Pers : Fr.) on fresh-market tomatoes with Bacillus amyloliquefaciens. Crop Prot 15 : 699 705.
45. McKnight SE. Effects of Bacillus subtilis on Cotton Seedling Development. Nottingham, UK, University of Nottingham, 1993 (PhD thesis).
46. Mellado EE, Moore RB, Nieto JJ, Ventosa A 1996) Analysis of 16S RNAr, gene sequences of Vibrio costicola strains: description of Salinivibrio costicola gen.nov., comb.nov. Int J Syst Bacteriol 46 : 817 821.
47. Mollet C, Drancourt M, Raoult D 1997) rpoB sequence analysis as a novel basis for bacterial identification. Mol Microbiol 26 : 1005 1011.
48. Muninbazi C, Bullerman LB 1998) Isolation and partial characterization of antifungal metabolites of Bacillus pumilus. J Appl Microbiol 84 : 959 968.
49. Niehaus F, Bertoldo C, Kahler M, Antranikian G 1999) Extremophiles as a source of novel enzymes for industrial applications. Appl Microbiol Biotechnol 51 : 711 729
50. Pandey A., Nigam P, Soccol CR, Soccol VT, Singh D, Monhan R 2000) Advances in microbiol amylases. Biotechnol Appl Biochem 31 : 35 152
51. Pleban S., Chernin L, Shet I 1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett Appl Microbiol 25 : 284 288.
52. Powell KA, Faull JL, Renwick A. The commercial and regulatory challenge. In : Hornby D (ed. Biological Control of Soil-borne Plant Pathogens. Wallingford, Oxon, UK, CAB International, 1990, pp. 445 463.
53. Pratella G, Mari M. Biologia e tecnica post-raccolta della melanzana, peperone e pomodoro. In : Prodotii Ortivi allo Stato Fresco: Biologia e tcnica post-raccolta. Cesena, Italy, 1990, pp. 4 23
54. Quesada E., Ventosa A, Rodriguez-Valera F, Ramos-Cormenzana A 1982) Types and properties of some bacteria isolated from hypersaline soils. J Appl Microbiol 53 : 155 161.
55. Rao MB, Tanksale AM, Ghatge MS, Deshpande VV 1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62 : 597 635
56. Renesto P., Gouvernet J, Drancourt M, Roux V, Raoult D 2000) Use of rpoB gene analysis for detection and identification of Bartonella species. J Clin Microbiol 39 : 430 437.
57. Rodriguez-Kabana R, Godoy G, Morgan-Jones G, Shelby RA 1983) the determination of soil chitinase activity: conditions for assay and ecological studies. Plant Soil 75 : 95 106.
58. Sadfi N, Cherif M, Fliss I, Boudabous A, Antoun H 2001) Evaluation of Bacillus isolates from salty soils and Bacillus thuringiensis strains for the biocontrol of Fusarium dry rot of potato tubers. J Plant Pathol 83 : 101 118.
59. Sadfi N, Cherif M, Hajlaoui MR, Boudabous A 2002) Biological control of the potato tubers dry rot caused by Fusarium roseum var. sambucinum under greenhouse, field and storage conditions using Bacillus spp. isolates. J Phytopathol 150 : 640 648.
60. Saitou N, Nei M 1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 : 406 425.
61. Sanchez-Porro C, Martin-Rengel S, Melado E, Bertoldo C, Antranikian G, Ventosa A. Extracellular Enzymes Produced by Moderately Halophilic Bacteria. Proc. Int Conf on Halophilic Microorganisms, Sevilla, Spain, 23-27 September, 2001, p. 51
62. Sanchez-Porro C., Martin S, Mellado E, Ventosa A 2003) Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J Appl Microbiol 94 : 295 300.
63. Shapira R, Ordentlich A, Chet I, Oppenheim AB 1989) Control of plant diseases by chitinase expressed from cloned DNA in Escherichia coli. Phytopathology 79 : 1246 1249.
64. Sierra GA 1957) Simple method for the selection pf lipolytic activity of microorganisms and some observations on the influence of the contact between cells and fatty substrates. Antonie van Leewenhoek 23 : 15 22.
65. Skerman VBD. A Guide to the Identification of the Genera of Bacteria, 1st edn. Baltimore, MD, USA, Williams and Wilkins, 1967.
66. Spring S, Ludwig W, Marquez MC, Ventosa A, Schleifer K-H 1996) Halobacillus gen. nov., with descriptions of Halobacillus litoralis sp. nov. and Halobacillus trueperi sp. nov. and transfer of Sporosarcina halophila to Halobacillus comb. nov. Int J Syst Bacteriol 46 : 492 496.
67. Takayanagi T, Ajisaka K, Takiguchi Y, Shimahara K 1991) Isolation and characterization of thermostable chitinases from Bacillus licheniformis X-7u. Biochem Biophys Acta 1078 : 404 410.
68. Tindall BJ. The Family Halobacteriaceae. In : Balows A, Trüper HG, Harder W, Schleifer KH (eds), The Prokaryotes. A Handbook of Bacteria: Ecophysiology, Isolation, Identification, Application, 2nd edn, Vol. 1, New York, NY, USA, Springer, 1992, pp. 768 808.
69. Trachuk LA, Revina LP, Shemyakina TM, Chestukhina GG, Stepanov VM 1996) Chitinases of Bacillus licheniformis B-6839: isolation and properties. Can J Microbiol 42 : 307 315.
70. Utkhede RS, Bogdanoff C, McNevin J 2001) Effects of biological and chemical treatments on Botrytis stem canker and fruit yield of tomato under greenhouse conditions. Can J Plant Pathol 23 : 253 259.
71. Van de Peer Y, De Wachter R 1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comp Appl Biosci 10 : 569 570.
72. Ventosa A, Nieto JJ, Oren A 1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62 : 504 544.
73. Walker R, Powel AA, Seddon B 1998) Bacillus isolates from the spermosphere of peas and dwarf French beans with antifungal activity against Botrytis cinerea and Pythium species. J Appl Microbiol 84 : 791 801.
74. 1 in chitin degradation. J Bacteriol 172 : 4017 4022.
75. Whipps JM 1987) Effect of media on growth and interactions between a range of soil-borne glasshouse pathogens and antagonistic fungi. New Phytol 107 : 127 142.
76. Winker S, Woese CR 1991) A definition of the domains Archae, bacteria and Eucarya in terms of small subunit ribosomal RNA characteristics. Syst Appl Microbiol 13 : 161 165.
77. Wisniewski ME, Wilson CL 1992) Biological control of postharvest diseases of fruits and vegetables: recent advances. HortScience 27 : 94 98.
78. Xu Y, Feller G, Gerday C, Glandorff N 2003) Metabolic enzymes from psychrophilic bacteria: challenge of adaptation to low temperatures in ornithine carbamoyltransferase from Morytellaabyssi. J Bacteriol 185 : 2161 2168.
79. Yourman LF, Jeffers SN 1999) Resistance to benzimidazole and dicarboximide fungicides in greenhouse isolates of Botrytis cinerea. Plant Dis 83 : 569 575.
80. Zhao J, Kong F 2003) Biocontrol activity against Botrytis cinerea by Bacillus subtilis 728 isolated from marine environment. Ann Microbiol 53 : 29 35.