1887

Chapter 5 : Bacteriophages for Control of Phytopathogens in Food Production Systems

Authors: Antonet M. Svircev1, Alan J. Castle2, Susan M. Lehman3
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Agriculture and Agri-Food Canada, 4902 Victoria Avenue North, P.O. Box 6000, Vineland Station, Ontario L0R 2E0, Canada; 2: Department of Biological Sciences, Brock University, 500 Glenridge Avenue, St. Catharines, Ontario L2S 3A1, Canada; 3: Centers for Disease Control and Prevention, 1600 Clifton Road NE, Mail Stop C-16, Atlanta, GA 30333
Content Type: Monograph
Publication Year: 2010

Category: Applied and Industrial Microbiology

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Bacteriophages for Control of Phytopathogens in Food Production Systems, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap05-2.gif

Abstract:

This chapter discusses some of the novel methods and technologies implemented in the search for phage biopesticides in agricultural food production systems. It is divided according to agriculturally related application lines. The first section summarizes the historic and current state of phage biopesticides. Most control strategies focus on the suppression of populations in the flower. This is followed by discussions of specific pathogens and application environments in which phages have been used. The third section examines the impact of bacteriophages on soil bacteria located in the rhizosphere and phylloplane, and the potential consequences to plant health and yield. The final section discusses general points to consider for the development of phage biopesticides in agriculture. The bulk of phage therapeutic research and commercial development focuses on the prevention of human pathogens in the food production pipeline. In the current regulatory environment, these types of phage therapies would have difficulty passing through the regulatory system. The success of a phage therapy against any particular disease also depends on the availability of many phages that, together, are effective against most or all strains of the causative agent.

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Bacteriophages for Control of Phytopathogens in Food Production Systems
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-1,webId=/content/author/10.1128/9781555816629.ch05-1,properties={foaf_givenname=Antonet M., foaf_name=Antonet M. Svircev, foaf_surname=Svircev, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-2,webId=/content/author/10.1128/9781555816629.ch05-2,properties={foaf_givenname=Alan J., foaf_name=Alan J. Castle, foaf_surname=Castle, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-3,webId=/content/author/10.1128/9781555816629.ch05-3,properties={foaf_givenname=Susan M., foaf_name=Susan M. Lehman, foaf_surname=Lehman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff3]]}]]
Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
/content/10.1128/9781555816629.ch05.ch05fig01
FIGURE 1
sp. phage biopesticides isolated from orchard environment belong to the (left), (bottom right), and (top right). Marker = 100 nm.
10.1128/9781555816629/f0084-01_thmb.gif
10.1128/9781555816629/f0084-01.gif
Image of FIGURE 1
FIGURE 1

sp. phage biopesticides isolated from orchard environment belong to the (left), (bottom right), and (top right). Marker = 100 nm.

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig02
FIGURE 2
Sequential processes and decisions made for the isolation of bacteriophage carrier isolates. Isolates were selected on the basis of culturability and ability to produce high-titer phage solutions with sp. bacteriophages in the culture collection. (Adapted from .)
10.1128/9781555816629/f0085-01_thmb.gif
10.1128/9781555816629/f0085-01.gif
Image of FIGURE 2
FIGURE 2

Sequential processes and decisions made for the isolation of bacteriophage carrier isolates. Isolates were selected on the basis of culturability and ability to produce high-titer phage solutions with sp. bacteriophages in the culture collection. (Adapted from .)

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig03
FIGURE 3
Effect of phage-carrier combinations on disease severity in forced pear blossom assays, given as mean ± 95% confidence limits for three replications (10 blossoms per replication). Four phages were applied with the carrier using a multiplicity of infection (MOI) of 2 and then again using an MOI of 20. These eight phage treatments, along with the carrier and phosphate buffer (PB) control, were repeated twice: once where 3 h elapsed between treatment and pathogen application (left-hand side) and once where the pathogen was applied immediately after treatment (right-hand side). All phage and carrier treatments except those marked with ‡ resulted in significantly less severe disease than the PB control. Phage-carrier treatments marked with * were significantly better than the carrier alone.
10.1128/9781555816629/f0086-01_thmb.gif
10.1128/9781555816629/f0086-01.gif
Image of FIGURE 3
FIGURE 3

Effect of phage-carrier combinations on disease severity in forced pear blossom assays, given as mean ± 95% confidence limits for three replications (10 blossoms per replication). Four phages were applied with the carrier using a multiplicity of infection (MOI) of 2 and then again using an MOI of 20. These eight phage treatments, along with the carrier and phosphate buffer (PB) control, were repeated twice: once where 3 h elapsed between treatment and pathogen application (left-hand side) and once where the pathogen was applied immediately after treatment (right-hand side). All phage and carrier treatments except those marked with ‡ resulted in significantly less severe disease than the PB control. Phage-carrier treatments marked with * were significantly better than the carrier alone.

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig04
FIGURE 4
Incidence of fire blight in a 4-year-old Gala apple orchard. Posttreatment, trees treated with buffer (controls) and all active treatments were artificially inoculated with 10 CFU/ml of BlightBan C9-1 (commercial biological control agent), two carrier-phage treatments, and streptomycin treatments marked with * caused significant reduction in disease incidence relative to the control (P < 0.01). The phage carrier was the orchard-isolated EH21-5. (Reprinted with permission of S. M. Lehman.)
10.1128/9781555816629/f0087-01_thmb.gif
10.1128/9781555816629/f0087-01.gif
Image of FIGURE 4
FIGURE 4

Incidence of fire blight in a 4-year-old Gala apple orchard. Posttreatment, trees treated with buffer (controls) and all active treatments were artificially inoculated with 10 CFU/ml of BlightBan C9-1 (commercial biological control agent), two carrier-phage treatments, and streptomycin treatments marked with * caused significant reduction in disease incidence relative to the control (P < 0.01). The phage carrier was the orchard-isolated EH21-5. (Reprinted with permission of S. M. Lehman.)

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig05
FIGURE 5
Electron micrographs showing (left) the infection of sp. bacterium by phages, and (right) individual phages belonging to the (top right) and (bottom right). Marker = 100 nm. (Courtesy of B. Balogh and J. Jones.)
10.1128/9781555816629/f0089-01_thmb.gif
10.1128/9781555816629/f0089-01.gif
Image of FIGURE 5
FIGURE 5

Electron micrographs showing (left) the infection of sp. bacterium by phages, and (right) individual phages belonging to the (top right) and (bottom right). Marker = 100 nm. (Courtesy of B. Balogh and J. Jones.)

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig06
FIGURE 6
Effect of formulations on the survival of sp. bacteriophages in the tomato canopy under field conditions. Experimental groups are distinguished as Silwet (circle), casein (diamond), pregelatinized corn flour (triangle), and nonformulated (square). (Reprinted with permission of B. Balogh and J. Jones.)
10.1128/9781555816629/f0090-01_thmb.gif
10.1128/9781555816629/f0090-01.gif
Image of FIGURE 6
FIGURE 6

Effect of formulations on the survival of sp. bacteriophages in the tomato canopy under field conditions. Experimental groups are distinguished as Silwet (circle), casein (diamond), pregelatinized corn flour (triangle), and nonformulated (square). (Reprinted with permission of B. Balogh and J. Jones.)

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816629.ch05.ch05fig07
FIGURE 7
The biopesticide value chain was developed at Agriculture and Agri-Food Canada by S. Boyetchko. The chain summarizes the multistep sequential processes and the go/no-go decision processes required in the development of a biopesticide. The main steps in the chain involve bioprospecting, determination of biological and environmental fate, biopesticide optimization, and technology scale-up. (Reprinted from with permission of the publisher.)
10.1128/9781555816629/f0096-01_thmb.gif
10.1128/9781555816629/f0096-01.gif
Image of FIGURE 7
FIGURE 7

The biopesticide value chain was developed at Agriculture and Agri-Food Canada by S. Boyetchko. The chain summarizes the multistep sequential processes and the go/no-go decision processes required in the development of a biopesticide. The main steps in the chain involve bioprospecting, determination of biological and environmental fate, biopesticide optimization, and technology scale-up. (Reprinted from with permission of the publisher.)

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816629.ch05
1. Abedon, S. T. 1989. Selection for bacteriophage latent period length by bacterial density: a theoretical examination. Microb. Ecol. 18: 79– 88.
2. Abedon, S. T. 2003. Bacteriophages could fight plant pathogens. Ind. Bioprocessing 25: 7.
3. Abuladze, T.,, M. Li,, M. Y. Menetrez,, T. Dean,, A. Senecal, and, A. Sulakvelidze. 2008. Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microbiol. 74: 6230– 6238.
4. Adams, M. H. 1959. Bacteriophages, p. 443– 522. Interscience Publishers, New York, NY.
5. Anal, A. K., and, H. Singh. 2007. Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends Food Sci. 18: 240– 251.
6. Ashelford, K. E.,, M. J. Day,, M. J. Bailey,, A. K. Lilley, and, J. C. Fry. 1999a. In situ population dynamics of bacterial viruses in a terrestrial environment. Appl. Environ. Microbiol. 65: 169– 174.
7. Ashelford, K. E.,, M. J. Day, and, J. C. Fry. 2003. Elevated abundance of bacteriophage infecting bacteria in soil. Appl. Environ. Microbiol. 69: 285– 289.
8. Ashelford, K. E.,, J. C. Fry,, J. M. Bailey,, A. R. Jeffries, and, M. J. Day. 1999b. Characterization of six bacteriophages of Serratia liquefaciens CP6 isolated from sugar beet phytosphere. Appl. Environ. Microbiol. 65: 1959– 1965.
9. Ashelford, K. E.,, S. J. Norris,, J. C. Fry,, M. J. Bailey, and, M. J. Day. 2000. Seasonal population dynamics and interactions of competing bacteriophages and their host in the rhizosphere. Appl. Environ. Microbiol. 66: 4193– 4199.
10. Bailey, K. L.,, S. M. Boyetchko,, G. Peng,, R. K. Hynes,, W. G. Taylor, and, W. M. Pitt. 2009. Developing weed control techniques with fungi, p. 1– 44. In M. Rai ( ed.), Advances in Fungal Biotechnology. I.K. International Private Ltd., New Delhi, India.
11. Balogh, B. 2002. Strategies of improving the efficacy of bacteriophages for controlling bacterial spot of tomato. M.S. thesis. University of Florida, Gainesville, FL.
12. Balogh, B. 2006. Characterization and use of bacteriophages associated with citrus bacterial pathogens for disease control. Ph.D. thesis. University of Florida, Gainesville, FL.
13. Balogh, B.,, B. I. Canteros,, R. E. Stall, and, J. B. Jones. 2008. Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis. 92: 1048– 1052.
14. Balogh, B.,, J. B. Jones,, M. T. Momol, and, S. M. Olson. 2005. Persistence of bacteriophages as biocontrol agents in the tomato canopy. Acta Hortic. 695: 299– 302.
15. Balogh, B.,, J. B. Jones,, M. T. Momol,, S. M. Olson,, A. Obradovic,, P. King, and, L. E. Jackson. 2003. Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis. 87: 949– 954.
16. Barnet, Y. M. 1972. Bacteriophages of Rhizobium trifolii. J. Gen. Virol. 15: 1– 15.
17. Barnet, Y. M., and, J. M. Vincent. 1970. Lysogenic conversion of Rhizobium trifolii. J. Gen. Microbiol. 61: 319– 325.
18. Bashan, Y.,, G. Holguin, and, L. E. de-Bashan. 2004. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can. J. Microbiol. 50: 521– 577.
19. Beattie, G. A., and, S. E. Lindow. 1994. Comparison of behavior of epiphytic fitness mutants of Pseudomonas syringae under controlled and field conditions. Appl. Environ. Microbiol. 60: 3799– 3808.
20. Behle, R. W.,, M. R. McGuire, and, B. S. Shasha. 1996. Extending the residual toxicity of Bacillus thuringiensis with casein-based formulations. J. Econ. Entomol. 89: 1399– 1405.
21. Bigwood, T.,, J. A. Hudson, and, C. Billington. 2009. Influence of host and bacteriophage concentrations on the inactivation of food-borne pathogenic bacteria by two phages. FEMS Microbiol. Lett. 291: 59– 64.
22. Billing, E. 1987. Avirulent mutants of Erwinia amylovora; relationship between phage sensitivity and biological properties. Plant Pathog. Bact. 4: 617– 622.
23. Bonn, W. G., and, T. van der Zwet. 2000. Distribution and economic importance of fire blight. p. 37– 53. In J. L. Vanneste ( ed.), Fire Blight: the Disease and Its Causative Agent, Erwinia amylovora. CABI Publishing, Wallingford, United Kingdom.
24. Borysowski, J.,, B. Weber-Dabrowska, and, A. Gorski. 2006. Bacteriophage endolysins as a novel class of antibacterial agents. Exp. Biol. Med. (Maywood) 231: 366– 377.
25. Boyer, M.,, J. Haurat,, S. Samain,, B. Segurens,, F. Gavory,, V. Gonzalez,, P. Mavingui,, R. Rohr,, R. Bally, and, F. Wisniewski-Dye. 2008. Bacteriophage prevalence in the genus Azospirillum and analysis of the first genome sequence of an Azospirillum brasilense integrative phage. Appl. Environ. Microbiol. 74: 861– 874.
26. Bradley, D. E. 1965. The morphology and physiology of bacteriophages as revealed by the electron microscope. J. R. Microsc. Soc. 84: 257– 316.
27. Brüssow, H., and, E. Kutter. 2005. Genomics and evolution of tailed phages, p. 91– 128. In E. Kutter and, A. Sulakvelidze ( ed.), Bacteriophages: Biology and Applications. CRC Press, Boca Raton, FL.
28. Cairns, B., and, R. J. Payne. 2008. Bacteriophage therapy and the mutant selection window. Antimicrob. Agents Chemother. 52: 4344– 4350.
29. Canchaya, C.,, G. Fournous, and, H. Brüssow. 2004. The impact of prophages on bacterial chromosomes. Mol. Microbiol. 53: 9– 18.
30. Chanishvili, N.,, T. Chanishvili,, M. Tediashvili, and, P. A. Barrow. 2001. Phages and their application against drug-resistant bacteria. J. Chem. Technol. Biotechnol. 76: 689– 699.
31. Chen, J., and, P. Novick. 2009. Phage-mediated intergeneric transfer of toxin genes. Science 323: 139– 141.
32. Civerolo, E. L. 1973. Relationship of Xanthomonas pruni bacteriophages to bacterial spot disease in Prunus. Phytopathology 63: 1279– 1284.
33. Civerolo, E. L., and, H. L. Keil. 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59: 1966– 1967.
34. Clark, J. R., and, J. B. March. 2006. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol. 24: 212– 218.
35. Clokie, M., R. J., and, A. M. Kropinski (ed.). 2009. Bacteriophages: Methods and Protocols, vol. 1. Isolation, Characterization, and Interactions. Vol. 2, Molecular and Applied Aspects. Humana Press, Springer, New York, NY.
36. Crosse, J. E., and, M. K. Hingorani. 1958. Method for isolating Pseudomonas mors-prunorum phages from the soil. Nature 181: 60– 61.
37. Day, M. J., and, R. V. Miller. 2008. Phage ecology of terrestrial environments, p. 281– 301. In S. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
38. Demolon, A., and, A. Dunez. 1936. Nouvelles observations sur le bactériophage et la fatique des sols cultiveés en Luzerne. Ann. Agron. 6: 435– 455.
39. d’Hérelle, F. 1917. Sur un microbe invisible antagonistic des bacilles dysentériques. C. R. Acad. Sci. Ser. D 165: 373– 375.
40. d’Hérelle, F. 1921. Le Bactériophage: Son Rôle dans l’Immunité. Masson, Paris, France.
41. Dougherty, E., M., K., P. Guthrie, and, M. Shapiro. 1996. Optical brighteners provide baculovirus activity enhancement and UV radiation protection. Biol. Control 7: 71– 74.
42. Dowd, S. E.,, S. D. Pillai,, S. Wang, and, M. Y. Corapcioglu. 1998. Delineating the specific influence of virus isoelectric point and size on virus adsorption and transport through sandy soils. Appl. Environ. Microbiol. 64: 405– 410.
43. Duckworth, D. H. 1987. History and basic properties of bacterial viruses, p. 1– 44. In S. M. Goyal,, C. P. Gerba, and, G. Bitton (ed.), Phage Ecology. John Wiley & Sons, New York, NY.
44. EBI Food Safety. 2006. LISTEX™ P100 phages for control of Listeria approved by US FDA as GRAS. October 24. EBI Food Safety, Wageningen, The Netherlands. http://www.ebifoodsafety.com/images/LISTEX%20receives%20FDA%20GRAS_Oct%2024%202006.pdf.
45. Erskine, J. M. 1973. Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemiology of fire blight. Can. J. Microbiol. 19: 837– 845.
46. Evans, J.,, Y. M. Barnet, and, J. M. Vincent. 1979. Effect of bacteriophage on the colonisation and nodulation of clover roots by a strain of Rhizobium trifolii. Can. J. Microbiol. 25: 968– 973.
47. Fischetti, V. A. 2008. Bacteriophage lysins as effective antibacterials. Curr. Opin. Microbiol. 11: 393– 400.
48. Flaherty, J. E.,, B. K. Harbaugh,, J. B. Jones,, G. C. Somodi, and, L. E. Jackson. 2001. H-mutant bacteriophages as a potential biocontrol of bacterial blight of geranium. HortScience 36: 98– 100.
49. Flaherty, J. E.,, J. B. Jones,, B. K. Harbaugh,, G. C. Somodi, and, L. E. Jackson. 2000. Control of bacterial spot on tomato in the greenhouse and field with H-mutant bacteriophages. Hort-Science 35: 882– 884.
50. Garcia, P.,, B. Martinez,, J. M. Obeso, and, A. Rodriguez. 2008. Bacteriophages and their application in food safety. Lett. Appl. Microbiol. 47: 479– 485.
51. Gill, J. J. 2000. Biological control of Erwinia amylovora using bacteriophages. M.S. thesis. Brock University, St. Catharines, Ontario, Canada.
52. Gill, J. J.,, T. Hollyer, and, P. M. Sabour. 2007. Bacteriophages and phage-derived products as antibacterial therapeutics. Expert Opin. Ther. Pat. 17: 1341– 1350.
53. Gill, J. J.,, A. M. Svircev,, R. Smith, and, A. J. Castle. 2003. Bacteriophages of Erwinia amylovora. Appl. Environ. Microbiol. 69: 2133– 2138.
54. Goodridge, L. D. 2004. Bacteriophage biocontrol of plant pathogens: fact or fiction? Trends Biotechnol. 22: 384– 385.
55. Goyer, C. 2005. Isolation and characterization of phages Stsc1 and Stsc3 infecting Streptomyces scabiei and their potential as biocontrol agents. Can. J. Plant Pathol. 27: 210– 216.
56. Guenther, S.,, D. Huwyler,, S. Richard, and, M. J. Loessner. 2009. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microbiol. 75: 93– 100.
57. Hagens, S., and, M. J. Loessner. 2007. Application of bacteriophages for detection and control of foodborne pathogens. Appl. Microbiol. Biotechnol. 76: 513– 519.
58. Hagens, S., and, M. L. Offerhaus. 2008. Bacteriophages—new weapons for food safety. Food Technol. 62: 46.
59. Harbaugh, B. K.,, J. B. Jones,, J. E. Flaherty, and, L. E. Jackson. 1998. Beneficial viruses—new allies in the fight against bacterial diseases. GrowerTalks 62: 84– 88.
60. Hildebrand, M., C., C. Tebbe, and, K. Geider. 2001. Survival studies with the fire blight pathogen Erwinia amylovora in soil and in a soil-inhabiting insect. J. Phytopathol. 149: 635– 639.
61. Hudson, J. A.,, C. Billington,, G. Carey-Smith, and, G. Greening. 2005. Bacteriophages as biocontrol agents in food. J. Food Prot. 68: 426– 437.
62. Ignoffo, C. M., and, C. Garcia. 1992. Combinations of environmental factors and simulated sunlight affecting activity of inclusion bodies of the Heliothis (Lepidoptera: Noctuidae) nucleopolyhedrosis virus. Environ. Entomol. 21: 210– 213.
63. Ignoffo, C. M., and, C. Garcia. 1994. Antioxidant and oxidative enzyme effects on the inactivation of inclusion bodies of the Heliothis baculovirus by simulated sunlight-UV. Environ. Entomol. 23: 1025– 1029.
64. Ignoffo, C. M., and, C. Garcia. 1995. Aromatic/heterocyclic amino acids and the stimulated sunlight-UV inactivation of the Heliothis/ Helicoverpa baculovirus. Environ. Entomol. 24: 480– 482.
65. Ignoffo, C. M.,, C. García, and, S. G. Saathoff. 1996. Sunlight stability and rain-fastness of formulations of baculovirus Heliothis. Environ. Entomol. 26: 1470– 1474.
66. Iriarte, F. B.,, B. Balogh,, M. T. Momol,, L. M. Smith,, M. Wilson, and, J. B. Jones. 2007. Factors affecting survival of bacteriophage on tomato leaf surfaces. Appl. Environ. Microbiol. 73: 1704– 1711.
67. Jackson, L. E. May 1989. Bacteriophage prevention and control of harmful plant bacteria. U.S. patent 4,828,999.
68. Johnson, K. B., and, V. O. Stockwell. 2000. Biological control of fire blight, p. 319– 337. In J. L. Vanneste (ed.), Fire Blight: the Disease and Its Causative Agent, Erwinia amylovora. 2000. CABI Publishing, Wallingford, United Kingdom.
69. Jones, J. B.,, L. E. Jackson,, B. Balogh,, A. Obradovic,, F. B. Iriarte, and, M. T. Momol. 2007. Bacteriophages for plant disease control. Annu. Rev. Phytopathol. 45: 245– 262.
70. Jones, J. B.,, M. T. Momol,, A. Obradovic,, B. Balogh, and, S. M. Olson. 2005. Bacterial spot management on tomatoes. Acta Hortic. 695: 119– 124.
71. Joseph, M. V.,, J. D. Desai, and, A. J. Desai. 1985. Possible involvemnt of phage-like structures in antagonism of cowpea rhizobia by Rhizobium trifolii. Appl. Environ. Microbiol. 49: 459– 461.
72. Katznelson, H., and, J. K. Wilson. 1941. Occurrence of Rhizobium meliloti bacteriophages. Soil Sci. 51: 59– 63.
73. Keel, C.,, Z. Ucurum,, P. Michaux,, M. Adrian, and, D. Haas. 2002. Deleterious impact of a virulent bacteriophage on survival and biocontrol activity of Pseudomonas fluorescens strain CHA0 in natural soil. Mol. Plant Microbe Interact. 15: 567– 576.
74. Keil, H. L., and, R. A. Wilson. 1963. Control of peach bacterial spot by Xanthomonas pruni bacteriophage. Phytopathology 53: 746– 747. (Abstract.)
75. Kim, W.-S.,, H. Salm, and, K. Geider. 2004. Expression of bacteriophage ϕEa1h lysozyme in Escherichia coli and its activity in growth inhibition of Erwinia amylovora. Microbiology 150: 2707– 2714.
76. Kleczkowska, J. 1950. Phage resistant mutants of Rhizobium trifolii. J. Gen. Microbiol. 4: 298– 310.
77. Kowalski, M.,, G. E. Ham,, L. R. Frederick, and, I. C. Anderson. 1974. Relationship between strains of Rhizobium japonicum and their bacteriophages from soil and nodules of field grown soybeans. Soil Sci. 118: 221– 228.
78. Kumhar, S. R., and, K. Ramkrishna. 2007. Symbiotic effectivity of phage resistant mutants of mothbean Rhizobium on different host genetic systems. J. Food Legumes 20: 83– 86.
79. Kutter, E., and, A. Sulakvelidze (ed.). 2005. Bacteriophages: Biology and Applications. CRC Press, Boca Raton, FL.
80. Lameiro, M. H.,, R. Malpique,, A. C. Silva,, P. M. Alves, and, E. Melo. 2006. Encapsulation of adenoviral vectors into chitosan-bile salt microparticles for mucosal vaccination. J. Biotechnol. 126: 152– 162.
81. Lang, J. M.,, D. H. Gent, and, H. F. Schwartz. 2007. Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis. 91:8 71– 878.
82. Lee, K. Y., and, T. R. Heo. 2000. Survival of Bifidobacterium longum immobilized in calcium alginate beads in simulated gastric juices and bile salt solution. Appl. Environ. Microbiol. 66: 869– 873.
83. Lehman, S. M. 2007. Development of a bacteriophage-based biopesticide for fire blight. Ph.D. thesis. Brock University, St. Catharines, Ontario, Canada.
84. Lehman, S. M.,, A. M. Kropinski,, A. J. Castle, and, A. M. Svircev. 2009. Complete genome of the broad-host-range Erwinia amylovora phage ΦEa21-4 and its relationship to Salmonella phage Felix O1. Appl. Environ. Microbiol. 75: 2139– 2147.
85. Ma, Y.,, J. C. Pacan,, Q. Wang,, Y. Xu,, X. Huang,, A. Korenevsky, and, P. M. Sabour. 2008. Microencapsulation of bacteriophage Felix O1 chitosan-alginate microspheres for oral cavity delivery. Appl. Environ. Microbiol. 74: 4799– 4805.
86. Marks, T., and, R. Sharp. 2000. Bacteriophages and biotechnology: a review. J. Clin. Technol. Biotechnol. 75: 6– 7.
87. Mattey, M., and, J. Spencer. 2008. Bacteriophage therapy—cooked goose or phoenix rising? Curr. Opin. Biotechnol. 19: 608– 612.
88. McNeil, D. L.,, S. Romero,, J. Kandula,, C. Stark,, A. Stewart, and, S. Larsen. 2001. Bacteriophages: a potential biocontrol agent against walnut blight (Xanthomonas campestris pv. juglandis). N. Z. Plant Prot. 54: 220– 224.
89. Moser, C. A.,, T. J. Speaker, and, P. A. Offit. 1998. Effect of water-based microencapsulation on protection against EDIM rotavirus challenge in mice. J. Virol. 72: 3859– 3862.
90. Munsch, P., and, J. M. Olivier. 1995. Biocontrol of bacterial blotch of the cultivated mushroom with lytic phages: some practical considerations. Mushroom Sci. 14: 595– 602.
91. Nechaeva, E. 2002. Development of oral microencapsulated forms for delivering viral vaccines. Expert Rev. Vaccines 1: 385– 397.
92. Obradovic, A.,, K. Gasic, and, M. Stepanovic. 2008. Bakteriofagi u zastiti bilja. (Bacteriophages in plant protection.) Biljni Lekar 36: 36– 44.
93. Obradovic, A.,, J. B. Jones,, M. T. Momol,, B. Balogh, and, S. M. Olson. 2004. Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Dis. 88: 736– 740.
94. Obradovic, A.,, J. B. Jones,, M. T. Momol,, S. M. Olson,, L. E. Jackson,, B. Balogh,, K. Guven, and, F. B. Iriarte. 2005. Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis. 89: 712– 716.
95. O’Brien, R. D., and, S. E. Lindow. 1989. Effect of plant species and environmental conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathology 79: 619– 627.
96. Offit, P. A.,, C. A. Khoury,, C. A. Moser,, H. F. Clark,, J. E. Kim, and, T. J. Speaker. 1994. Enhancement of rotavirus immunogenicity by microencapsulation. Virology 203: 134– 143.
97. Okabe, N., and, M. Goto. 1963. Bacteriophages of plant pathogens. Annu. Rev. Phytopathol. 1: 397– 418.
98. Rao, A. V.,, N. Shiwnarain, and, J. Maharaj. 1989. Survival of microencapsulated Bifidobacterium pseudolongum in simulated gastric and intestinal juices. Can. Inst. Food Sci. Technol.J. 22: 345– 349.
99. Ravensdale, M.,, T. J. Blom,, G. Gracia,, J. A. Garza,, A. M. Svircev, and, R. J. Smith. 2007. Bacteriophages and the control of Erwinia carotovora subsp. carotovora. Can.J. Plant Pathol. 29: 121– 130.
100. Ritchie, D. F. 1978. Bacteriophages of Erwinia amylovora: their isolation, distribution, characterization, and possible involvement in the etiology and epidemiology of fire blight. Ph.D. thesis. Michigan State University. East Lansing, MI.
101. Ritchie, D. F., and, E. J. Klos. 1977. Isolation of Erwinia amylovora bacteriophage from aerial parts of apple trees. Phytopathology 67: 101– 104.
102. Ritchie, D. F., and, E. J. Klos. 1979. Some properties of Erwinia amylovora bacteriophages. Phytopathology 69: 1078– 1083.
103. Roach, D. R.,, A. J. Castle,, A. M. Svircev, and, F. A. Tumini. 2008. Phage-based biopesticides: characterization of phage resistance and host range for sustainability. Acta Hortic. 793: 397– 401.
104. Saccardi, A.,, E. Gambin,, M. Zaccardelli,, G. Barone, and, U. Mazzucchi. 1993. Xanthomonas campestris pv. pruni control trials with phage treatments on peach in the orchard. Phytopathol. Mediterr. 32: 206– 210.
105. Schnabel, E. L.,, W. G. D. Fernando,, M. P. Meyer,, A. L. Jones, and, L. E. Jackson. 1999. Bacteriophage of Erwinia amylovora and their potential for biocontrol. Acta Hortic. 489: 649– 653.
106. Schnabel, E. L., and, A. L. Jones. 2001. Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora. Appl. Environ. Microbiol. 67: 59– 64.
107. Schroth, M. N., and, J. G. Hancock. 1981. Selected topics in biological control. Ann. Rev. Microbiol. 35: 453– 476.
108. Shapiro, M. 1992. Use of optical brighteners as radiation protectants for gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus. J. Econ. Entomol. 85: 1682– 1686.
109. Skurnik, M., and, E. Strauch. 2006. Phage therapy: facts and fiction. Int. J. Med. Microbiol. 296: 5– 14.
110. Smit, E.,, A. C. Wolters,, H. Lee,, J. T. Trevors, and, J. D. van Elsas. 1996. Interactions between a genetically marked Pseudomonas fluorescens strain and bacteriophage ΦR2f in soil: effects of nutrients, alginate encapsulation, and the wheat rhizosphere. Microbial Ecol. 31: 125– 140.
111. Srinivasiah, S.,, J. Bhavsar,, K. Thapar,, M. Liles,, T. Schoenfeld, and, K. E. Wommack. 2008. Phages across the biosphere: contrasts of viruses in soil and aquatic environments. Res. Microbiol. 159: 349– 357.
112. Stephens, P. M.,, M. O’Sullivan, and, F. Gara. 1987. Effect of bacteriophages on colonization of sugarbeet roots by fluorescent Pseudomonas spp. Appl. Environ. Microbiol. 53: 1164– 1167.
113. Stewart, A. 2001. Commercial biocontrol—reality or fantasy? Australas. Plant Pathol. 30: 127– 131.
114. Stewart, F. M., and, B. R. Levin. 1984. The population biology of bacterial viruses: why be temperate? Theor. Popul. Biol. 26: 93– 117.
115. Stone, R. 2002. Bacteriophage therapy. Food and agriculture: testing grounds for phage therapy. Science 298: 730.
116. Sturesson, C., and, L. Degling Wikingsson. 2000. Comparison of poly(acryl starch) and poly(lactide-co-glycolide) microspheres as drug delivery system for a rotavirus vaccine. J. Control. Release 68: 441– 450.
117. Subcommittee on Microbial Criteria, Committee on Food Protection, Food and Nutrition Board, National Research Council. 1985. An Evaluation of the Role of Microbiological Criteria for Foods and Food Ingredients. National Academy Press, Washington, DC.
118. Summers, W. C. 1999. Félix d’Hérelle and the Origins of Molecular Biology. Yale University Press, New Haven, CT.
119. Summers, W. C. 2001. Bacteriophage therapy. Annu. Rev. Microbiol. 55: 437– 451.
120. Summers, W. C. 2005. Bacteriophage research: early history, p. 5– 27. In E. Kutter and, A. Sulakvelidze (ed.), Bacteriophages: Biology and Applications. CRC Press, Boca Raton, FL.
121. Svircev, A. M.,, J. J. Gill, and, P. Sholberg. 2002a. Erwinia amylovora (Burrill) Winslow, Broadhurst, Buchanan, Krumwiede, Rogers and Smith, fire blight (Enterobacteriaceae), p. 448– 451. In P. G. Mason and, J. T. Huber (ed.), Biological Control Programmes in Canada, 1981–2000. CABI Publishing, Wallingford, United Kingdom.
122. Svircev, A. M.,, W. S. Kim,, S. M. Lehman, and, A. J. Castle. 2009. Erwinia amylovora: modern methods for detection and differentiation, p. 115– 129. In R. Burns (ed.), Methods in Molecular Biology. Humana Press, Clifton, NJ.
123. Svircev, A. M.,, S. M. Lehman,, W. S. Kim,, E. Barszcz,, K. E. Schneider, and, A. J. Castle. 2006. Control of the fire blight pathogen with bacteriophages, p. 259– 261. In W. Zeller and, C. Ullrich (ed.), Proceedings of the 1st International Symposium on Biological Control of Bacterial Plant Diseases. Arno Brynda, Berlin, Germany.
124. Svircev, A. M.,, R. Smith,, G. Gracia,, J. A. Garza,, J. J. Gill, and, K. Schneider. 2002b. Biocontrol of Erwinia with bacteriophages. IOBC/WPRS Bull. 25: 139– 142.
125. Tamez-Guerra, P.,, M. R. McGuire,, R. W. Behle,, B. S. Shasha, and, L. J. G. Wong. 2000. Assessment of microencapsulated formulations for improved residual activity of Bacillus thuringiensis. J. Econ. Entomol. 93: 219– 225.
126. Tan, J. S. H., and, D. C. Reanney. 1976. Interactions between bacteriophages and bacteria in soil. Soil. Biol. Biochem. 8: 145– 150.
127. Tanji, Y.,, T. Shimada,, H. Fukudomi,, K. Miyanaga,, Y. Nakai, and, H. Unno. 2005. Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J. Biosci. Bioeng. 100: 280– 287.
128. Tanji, Y.,, T. Shimada,, M. Yoichi,, K. Miyanaga,, K. Hori, and, H. Unno. 2004. Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl. Microbiol. Biotechnol. 64: 270– 274.
129. Taylor, D. H.,, R. S. Moore, and, L. S. Sturman. 1981. Influence of pH and electrolyte composition on adsorption of poliovirus by soils and minerals. Appl. Environ. Microbiol. 42: 976– 984.
130. Thiel, C. 2004. Old dogma, new tricks—21st century phage therapy. Nat. Biotechnol. 22: 31– 36.
131. Uludag, H.,, P. DeVos, and, P. A. Tresco. 2000. Technology of mammalian cell encapsulation. Adv. Drug Deliv. Rev. 42: 29– 64.
132. Vandenbergh, P. A., and, R. L. Cole. 1986. Cloning and expression in Escherichia coli of the polysaccharide depolymerase associated with bacteriophage-infected Erwinia amylovora. Appl. Environ. Microbiol. 51: 862– 864.
133. Vandenbergh, P. A.,, A. M. Wright, and, A. K. Vidaver. 1985. Partial purification and characterization of a polysaccharide depolymerase associated with phage-infected Erwinia amylovora. Appl. Environ. Microbiol. 49: 994– 996.
134. van der Zwet, T., and, S. V. Beer. 1995. Fire Blight—Its Nature, Prevention and Control: A Practical Guide to Integrated Disease Management. USDA agriculture information bulletin no. 631. U.S. Department of Agriculture, Washington, DC.
135. Vanneste, J. L. (ed.). 2000. Fire Blight: the Disease and Its Causative Agent, Erwinia amylovora. CABI Publishing, Wallingford, United Kingdom.
136. Vidaver, A. K. 1976. Prospects for control of phytopathogenic bacteria by bacteriophages and bacteriocins. Ann. Rev. Phytopathol. 14: 451– 465.
137. Vlachakis, J., and, M. Verhoyen. 1984. Isolation of Erwinia amylovora (Burrill) Winslow et al., bacteriophages to struggle against pear fireblight. Int. Symp. Fytofarmacie Fytiatrie 36: 551– 558.
138. Wang, I.-N.,, D. E. Dykhuizen, and, L. B. Slobodkin. 1996. The evolution of phage lysis timing. Evol. Ecol. 10: 545– 558.
139. Williams, K. E.,, J. B. Schnitker,, M. Radosevich,, D. W. Smith, and, K. E. Wommack. 2008. Cultivation-based assessment of lysogeny among soil bacteria. Microb. Ecol. 56: 437– 447.
140. Williams, S. T.,, A. M. Mortimer, and, L. Manchaster. 1987. Ecology of soil bacteriophages, p. 157– 179. In S. M. Goyal,, C. P. Gerba, and, G. Bitton (ed.), Phage Ecology. John Wiley & Sons, New York, NY.
141. Williamson, K. E.,, K. E. Wommack, and, M. Radosevich. 2003. Sampling natural viral communities from soil for culture-independent analyses. Appl. Environ. Microbiol. 69: 6628– 6633.
142. Wilson, M., and, S. E. Lindow. 2000. Implications of the viable but nonculturable state in risk assessment based on field testing of genetically engineered microorganisms, p. 229– 241. In R. R. Colwell and, D. J. Grimes (ed.), Nonculturable Microorganisms in the Environment. ASM Press, Washington, DC.
143. Zaccardelli, M.,, A. Saccardi,, E. Gambin, and, U. Mazzucchi. 1992. Xanthomonas campestris pv. pruni bacteriophages on peach trees and their potential use for biological control. Phytopathol. Mediterr. 31: 133– 140.

Tables

Bacteriophages for Control of Phytopathogens in Food Production Systems
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-1,webId=/content/author/10.1128/9781555816629.ch05-1,properties={foaf_givenname=Antonet M., foaf_name=Antonet M. Svircev, foaf_surname=Svircev, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-2,webId=/content/author/10.1128/9781555816629.ch05-2,properties={foaf_givenname=Alan J., foaf_name=Alan J. Castle, foaf_surname=Castle, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816629.ch05-3,webId=/content/author/10.1128/9781555816629.ch05-3,properties={foaf_givenname=Susan M., foaf_name=Susan M. Lehman, foaf_surname=Lehman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816629.ch05-aff3]]}]]
Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5
/content/10.1128/9781555816629.ch05.ch05tab01
TABLE 1
Effects of phage treatment on bacterial spot in peach orchards
Generic image for table
TABLE 1

Effects of phage treatment on bacterial spot in peach orchards

Citation: Svircev A, Castle A, Lehman S. 2010. Bacteriophages for Control of Phytopathogens in Food Production Systems, p 79-102. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch5

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error