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Crop Use of Bacteriophages

Abstract

Bacteriophages have been a focus of biological control activity in various crop systems since nearly their discovery in the early 1900s. Bacteriophage population sizes must be maintained at high levels in the phyllosphere – that is, the aboveground portions of plants – for effective disease control. Phage persistence, however, is adversely affected by various physical factors such as exposure to high levels of ultraviolet light. Various strategies have been used to increase the longevity of phages in the phyllosphere. Application of phages in the evening, or the use of various compounds mixed with phage solutions, has been shown to extend phage persistence on leaf surfaces. Skim milk was used in several studies, and the combination resulted in improved control of bacterial spot of tomato disease compared to the standard bactericide treatment. Another strategy for improving disease control is to use a carrier-phage system. The system uses a nonpathogenic bacterium to deliver the bacteriophages to the flower surface and simultaneously propagate the phage populations on the stigma surface. Field-based experiments have shown that the carrier-phage system can provide a significant control of the pathogen.

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References

  • Abbasi PA, Soltani N, Cuppels DA, Lazarovits G (2002) Reduction of bacterial spot disease severity on tomato and pepper plants with foliar applications of ammonium lignosulfonate and potassium phosphate. Plant Dis 86:1232–1236

    CrossRef  Google Scholar 

  • Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A (2008) Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl Environ Microbiol 74(20):6230–6238

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams MH (1959) Bacteriophages. Interscience Publishers, New York

    Google Scholar 

  • Balogh B (2002) Strategies of improving the efficacy of bacteriophages for controlling bacterial spot of tomato. MS thesis, University of Florida

    Google Scholar 

  • Balogh B (2006) Characterization and use of bacteriophages associated with citrus bacterial pathogens for disease control. Dissertation, University of Florida

    Google Scholar 

  • Balogh B, Jones JB, Momol MT, Olson SM, Obradovic A, King P et al (2003) Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis 87:949–954

    CrossRef  Google Scholar 

  • Balogh B, Canteros BI, Stall KE, Jones JB (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92:1048–1052

    CrossRef  Google Scholar 

  • Balogh B, Jones JB, Iriarte FB, Momol MT (2010) Phage therapy for plant disease control. Curr Pharm Biotechnol 11(1):48–57

    CrossRef  CAS  PubMed  Google Scholar 

  • Basim H, Minsavage GV, Stall RE, Wang JF, Shanker S, Jones JB (2005) Characterization of a unique chromosomal copper resistance gene cluster from Xanthomonas campestris pv. vesicatoria. Appl Environ Microbiol 71:8284–8291

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender CL, Cooksey DA (1986) Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance. J Bacteriol 165:534–541

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender CL, Cooksey DA (1987) Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato. J Bacteriol 169:470–474

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender CL, Malvick DK, Conway KE, George S, Cooksey DA (1990) Characterization of pXv10A, a copper resistance plasmid in Xanthomonas campestris pv. vesicatoria. Appl Environ Microbiol 56:170–175

    PubMed  PubMed Central  CAS  Google Scholar 

  • Boulé J, Sholberg PL, Lehman SM, O’Gorman DT, Svircev AM (2011) Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada. Can J Plant Pathol 33(3):308–317

    CrossRef  Google Scholar 

  • Brunoghe R, Maisin J (1921) Essais de therapeutique au moyen du bacteriophage du staphylocoque. C R Soc Biol 85:1020–1021

    Google Scholar 

  • Burrill TJ (1878) Pear blight. Trans Ill State Hortic Soc 11:114–116

    Google Scholar 

  • Byrne JM, Dianese AC, Ji P, Campbell HL, Cuppels DA, Louws FJ et al (2005) Biological control of bacterial spot of tomato under field conditions at several locations in North America. Biol Control 32:408–418

    CrossRef  Google Scholar 

  • Cairns B, Payne RJ (2008) Bacteriophage therapy and the mutant selection window. Antimicrob Agents Chemother 52:4344–4350

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Canteros BI (1999) Copper resistance in Xanthomonas campestris pv. citri. In: Proceedings of the 9th international conference on plant pathogenic bacteria, Madras, pp 455–459

    Google Scholar 

  • Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8:769–783

    CrossRef  CAS  PubMed  Google Scholar 

  • Civerolo EL (1973) Relationship of Xanthomonas pruni bacteriophages to bacterial spot disease in prunus. Phytopathology 63:1279–1284

    CrossRef  Google Scholar 

  • Civerolo EL, Keil HL (1969) Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59:1966–1967

    Google Scholar 

  • Coons GH, Kotila JE (1925) The transmissible lytic principle (bacteriophage) in relation to plant pathogens. Phytopathology 15:357–370

    Google Scholar 

  • Díaz-Muñoz SL, Koskella B (2014) Bacteria-Phage interactions in natural environments. Adv Appl Microbiol 89:135–183

    CrossRef  PubMed  Google Scholar 

  • Erskine JM (1973) Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemiology of fire blight. Can J Microbiol 19:837–845

    CrossRef  CAS  PubMed  Google Scholar 

  • Erskine JM, Lopatecki LE (1975) In vitro and in vivo interactions between Erwinia amylovora and related saprophytic bacteria. Can J Microbiol 21:35–41

    CrossRef  CAS  PubMed  Google Scholar 

  • Flaherty JE, Harbaugh BK, Jones JB, Somodi GC, Jackson LE (2001) H-mutant bacteriophages as a potential biocontrol of bacterial blight of geranium. Hortic Sci 36:98–100

    Google Scholar 

  • Frampton RA, Pitman AR, Fineran PC (2012) Advances in bacteriophage-mediated control of plant pathogens. Int J Microbiol 2012:1–12

    CrossRef  Google Scholar 

  • Fujiwara A, Fujisawa M, Hamasaki R, Kawasaki T, Fujie M, Yamada T (2011) Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Appl Environ Microbiol 77:4155–4162

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Gašic K, Ivanovic MM, Ignjatov M, Calic A, Obradovic A (2011) Isolation and characterization of Xanthomonas euvesicatoria bacteriophages. J Plant Pathol 93:415–423

    Google Scholar 

  • Gill JJ, Abedon ST (2003) Bacteriophage ecology and plants. http://www.apsnet.org/publications/apsnetfeatures/Pages/BacteriophageEcology.aspx

  • Gill JJ, Svircev AM, Smith R, Castle AJ (2003) Bacteriophages of Erwinia amylovora. Appl Environ Microbiol 69:2133–2138

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Goto M (1992) Fundamentals of bacterial plant pathology. Academic, San Diego

    Google Scholar 

  • Ignoffo CM, Garcia C (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

    CrossRef  Google Scholar 

  • Ignoffo CM, Garcia C (1994) Antioxidant and oxidative enzyme effects on the inactivation of inclusion bodies of the Helilotis baculovirus by simulated sunlight-UV. Environ Entomol 23(4):1025–1029

    CrossRef  CAS  Google Scholar 

  • Ignoffo CM, Rice WC, McIntosh AH (1989) Inactivation of non-occluded and occluded baculoviruses and baculovirus-DNA exposed to simulated sunlight. Environ Entomol 18:177–183

    CrossRef  Google Scholar 

  • Ignoffo CM, Shasha BS, Sharpio M (1991) Sunlight ultraviolet protection of the Heliothis Nuclear Polyhedrosis Virus through starch-encapsulation technology. J Invert Pathol 57:134–136

    CrossRef  Google Scholar 

  • Ignoffo CM, Garcia C, Saathoff SG (1997) Sunlight stability and rain-fastness of formulations of Baculovirus helilotis. Environ Entomol 26(6):1470–1474

    CrossRef  Google Scholar 

  • Iriarte FB, Balogh B, Momol MT, Smith LM, Wilson M, Jones JB (2007) Factors affecting survival of bacteriophage on tomato leaf surfaces. Appl Environ Microbiol 73:1704–1711

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Iriarte FB, Obradovic A, Wernsing MH, Jackson LE, Balogh B, Hong JA (2012) Soil-based systemic delivery and phyllosphere in vivo propagation of bacteriophages: two possible strategies for improving bacteriophage efficacy for plant disease control. Bacteriophage 2(4): 214–224. http://www.tandfonline.com/doi/full/10.4161/bact.23530#abstract

    CrossRef  Google Scholar 

  • Jackson LE, Jones JB, Momol MT, Ji P (2004) Bacteriophage: a viable bacteria control solution. In: Proceedings of first international symposium Tomato Dis Orlando, pp 21–24

    Google Scholar 

  • Ji P, Campbell HL, Kloepper JW, Jones JB, Suslow TV, Wilson M (2006) Integrated biological control of bacterial speck and spot of tomato under field conditions using foliar biological control agents and plant growth-promoting rhizobacteria. Biol Control 36:358–367

    CrossRef  Google Scholar 

  • Johnson KB (1994) Dose–response relationships and inundative biological control. Phytopathology 84:780–784

    Google Scholar 

  • Jones JB, Iriarte FB, Obradovic A, Balogh B, Momol MT, Jackson LE (2006) Management of bacterial spot on tomatoes with bacteriophages. In: Proceedings of the international symposium on biological control of bacterial plant diseases, 1st Darmstadt, vol 408, p 154

    Google Scholar 

  • Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB, Momol MT (2007) Bacteriophages for plant disease control. Annu Rev Phytopathol 45:245–262

    CrossRef  CAS  PubMed  Google Scholar 

  • Kasman LM, Kasman A, Westwater C, Dolan J, Schmidt MG, Norris JS (2002) Overcoming the phage replication threshold: a mathematical model with implications for phage therapy. J Virol 76:5557–5564

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotila JE, Coons GH (1925) Investigations on the blackleg disease of potato. Mich Agric Exp Stn Tech Bull 67:3–29

    Google Scholar 

  • Lang JM, Gent DH, Schwartz HF (2007) Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis 91(7):871–878

    CrossRef  CAS  Google Scholar 

  • Lehman SM (2007) Development of a bacteriophage-based biopesticide for fire blight. Dissertation, Brock University

    Google Scholar 

  • Lehman SM, Kropinski AM, Castle AJ, Svircev AM (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(7):2139–2147. https://doi.org/10.1128/aem.02352-08

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee YA, Hendson M, Panapoulos NJ, Schroth MN (1994) Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas campestris pv. juglandis: homology with small blue copper proteins and multicopper oxidase. J Bacteriol 176:173–188

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Louws EJ, Wilson M, Cambell HL, Cuppels DA, Jones JB, Shoemaker PB et al (2001) Field control of bacterial spot and bacterial speck of tomato using a plant activator. Plant Dis 85:481–488

    CrossRef  CAS  Google Scholar 

  • Mallmann WL, Hemstreet CJ (1924) Isolation of an inhibitory substance from plants. Agric Res 28:599–602

    Google Scholar 

  • Manulis S, Zutra D, Kleitman F, Dror O, David I, Zilberstaine M et al (1998) Distribution of streptomycin-resistant strains of Erwinia amylovora in Israel and occurrence of blossom blight in the autumn. Phytoparasitica 26:223–230

    CrossRef  Google Scholar 

  • Marco GM, Stall RE (1983) Control of bacterial spot of pepper initiated by strains of Xanthomonas campestris pv. vesicatoria that differ in sensitive to copper. Plant Dis 67:779–781

    CrossRef  CAS  Google Scholar 

  • McGuire MR, Shasha BS (1995) Starch encapsulation of microbial pesticides. In: Hall FR, Barry JW (eds) Biorational pest control agents: formulation and delivery. American Chemical Society, Washington, DC, pp 229–237

    CrossRef  Google Scholar 

  • McGuire MR, Shasha BS, Lewis LC, Bartelt RJ, Kinney K (1990) Field evaluation of granular starch formulations of Bacillus thuringiensis against Ostrinia nubialis (Lepidoptera: Pyralidae). J Econ Entomol 83(6):2207–2210

    CrossRef  Google Scholar 

  • McGuire MR, Shasha BS, Lewis LC, Nelsen TC (1994) Residual activity of granular starch-encapsulated Bacillus thuringiensis. J Econ Entomol 87(3):631–637

    CrossRef  Google Scholar 

  • McGuire MR, Behle RW, Shasha BS (1996) Starch and flour-based sprayable formulations: effect of rain fastness and solar stability of Bacillus thuringiensis. J Econ Entomol 89(5):863–869

    CrossRef  Google Scholar 

  • McNeil DL, Romero S, Kandula J, Stark C, Stewart A, Larsen S (2001) Bacteriophages: a potential biocontrol agent against walnut blight (Xanthomonas campestris pv. juglandis). N Z Plant Protect 54:220–224

    Google Scholar 

  • Moore ES (1926) d’Herelle’s bacteriophage in relation to plant parasites. S Afr J Sci 23:306

    Google Scholar 

  • Murugaiyan S, Bae JY, Wu J, Lee SD, Um HY, Choi HK, Lee JH, Lee SW (2011) Characterization of filamentous bacteriophage PE226 infecting Ralstonia solanacearum strains. J Appl Microbiol 110(1):296–303

    CrossRef  CAS  PubMed  Google Scholar 

  • Nagy JK, Schwarczinger I, Kuenstler A, Pogany M, Kiraly L (2015) Penetration and translocation of Erwinia amylovora-specific bacteriophages in apple – a possibility of enhanced control of fire blight. Eur J Plant Pathol 142(4):815–827

    CrossRef  CAS  Google Scholar 

  • Obradović A, Jones JB, Momol MT, Balogh B, Olson SM (2004) Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Dis 88:736–740

    CrossRef  Google Scholar 

  • Obradović A, Jones JB, Momol MT, Olson SM, Jackson LE, Balogh B (2005) Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis 89:712–716

    CrossRef  CAS  Google Scholar 

  • Obradović A, Jones JB, Balogh B, Momol MT (2008) Integrated management of tomato bacterial spot. In: Ciancio A, Mukerji G (eds) Integrated management of plant diseases caused by fungi, phytoplasma and bacteria. Springer Science + Business Media BV, Dordrecht, pp 211–223

    CrossRef  Google Scholar 

  • Okabe N, Goto M (1963) Bacteriophages of plant pathogens. Annu Rev Phytopathol 1:397–418

    CrossRef  Google Scholar 

  • Perera MN, Abuladze T, Li M, Woolston J, Sulakvelidze A (2015) Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiol 52:42–48

    CrossRef  CAS  PubMed  Google Scholar 

  • Primrose SB, Seeley ND, Logan K (1984) The recovery of viruses from water: methods and applications. In: Goddard M (ed) Viruses and wastewater treatment: proceedings of the international symposium on viruses and wastewater treatment, 15–17 September 1980. University of Surrey, Guildford, pp 211–234

    Google Scholar 

  • Ritchie D (1978) Bacteriophages of Erwinia amylovora: their isolation, distribution, characterization, and possible involvement in the etiology and epidemiology of fire blight. Dissertation, Michigan State University

    Google Scholar 

  • Ritchie DF, Klos EJ (1977) Isolation of Erwinia amylovora bacteriophage from aerial parts of apple trees. Phytopathology 67:101–104

    CrossRef  Google Scholar 

  • Roach DR, Sjaarda DR, Castle AJ, Svircev AM (2013) Host exopolysaccharide quantity and composition impact Erwinia amylovora bacteriophage pathogenesis. Appl Environ Microbiol 79:3249–3256

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Roach DR, Sjaarda DR, Sjaarda CP, Ayala CJ, Howcroft B, Castle AJ, Svircev AM (2015) Absence of lysogeny in wild populations of Erwinia amylovora and Pantoea agglomerans. Microb Biotechnol 8:510–518

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Schnabel EL, Jones AL (2001) Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora. Appl Environ Microbiol 67(1):59–64

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Solodovnikov YP, Pavlova LI, Emelyanov PI (1970) Prophylactic application of dry polyvalent dysentery bacteriophage with pectin in children’s preschool. Z Mikrobiol Epidemiol Immunobiol 47:131–137

    Google Scholar 

  • Stall RE, Loschke DC, Jones JB (1986) Linkage of copper resistance and avirulence loci on a self-transmissible plasmid in Xanthomonas campestris pv. vesicatoria. Phytopathology 76:240–243

    CrossRef  CAS  Google Scholar 

  • Storey MV, Ashbolt NJ (2001) Persistence of two model enteric viruses (B40-8 and MS-2 bacteriophages) in water distribution pipe biofilms. Water Sci Technol 43:133–138

    CrossRef  CAS  PubMed  Google Scholar 

  • Sulakvelidze A (2013) Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogens. J Sci Food Agric 93(13):3137–3146

    CrossRef  CAS  PubMed  Google Scholar 

  • Summers WC (2005) Bacteriophage research: early history. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, Boca Raton, pp 5–27

    Google Scholar 

  • Sundin GW, Bender CL (1993) Ecological and genetic analysis of copper and streptomycin resistance in Pseudomonas syringae pv. syringae. Appl Environ Microbiol 59:1018–1024

    PubMed  PubMed Central  CAS  Google Scholar 

  • Svircev AM, Castle AJ, Lehman SM (2010) Bacteriophages for control of phytopathogens in food production systems. In: Sabour PM, Griffiths MW (eds) Bacteriophages in the control of food- and waterborne pathogens. ASM Press, Washington, DC, pp 79–102

    CrossRef  Google Scholar 

  • Svircev AM, Boule J, Sholberg P, Castle AJ (2013) Erwinia amylovora (Burrill) Winslow et al., fire blight (Enterobacteriaceae). In: Mason PG, Gillespie DR (eds) Biological control programmes in Canada 2001–2012. CABI, Wallingford, pp 408–412

    CrossRef  Google Scholar 

  • Sykes IK, Lanning S, Williams ST (1981) The effect of pH on soil actinophage. J Gen Microbiol 122:271–280

    Google Scholar 

  • Tanaka H, Negishi H, Maeda H (1990) Control of tobacco bacterial wilt by an avirulent strain of Pseudomonas solanacearum M4S and its bacteriophage. Ann Phytopathol Soc Jpn 56:243–246

    CrossRef  Google Scholar 

  • Thayer PL, Stall RE (1961) A survey of Xanthomonas vesicatoria resistance to streptomycin. Proc Fla State Hortic Soc 75:163–165

    Google Scholar 

  • Thomas RC (1935) A bacteriophage in relation to Stewart’s disease of corn. Phytopathology 25:371–372

    Google Scholar 

  • Wiggins BA, Alexander A (1985) Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems. Appl Environ Microbiol 49:19–23

    PubMed  PubMed Central  CAS  Google Scholar 

  • Williams ST, Mortimer AM, Manchester L (1987) Ecology of soil bacteriophages. In: Goyal SM, Gerba CP, Bitton G (eds) Phage ecology. Wiley, New York, pp 157–179

    Google Scholar 

  • Wilson M, Campbell HL, Ji P, Jones JB, Cuppels DA (2002) Biological control of bacterial speck of tomato under field conditions at several locations in North America. Phytopathology 92:1284–1292

    CrossRef  CAS  PubMed  Google Scholar 

  • Wittmann J, Klumpp J, Moreno Switt A, Yagubi A, Ackermann H-W, Wiedmann M, Svircev A, Nash JE, Kropinski A (2015) Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily – “Enquartavirinae”. Arch Virol 160(12):3053–3062. https://doi.org/10.1007/s00705-015-2609-6

    CrossRef  PubMed  CAS  Google Scholar 

  • Yagubi AI, Castle AJ, Kropinski AM, Banks TW, Svircev AM (2014) Complete genome sequence of Erwinia amylovora bacteriophage vB_EamM_Ea35-70. Genome Announc 2:413–414

    CrossRef  Google Scholar 

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Jones, J.B., Svircev, A.M., Obradović, A.Ž. (2018). Crop Use of Bacteriophages. In: Harper, D., Abedon, S., Burrowes, B., McConville, M. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-40598-8_28-1

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