DOI QR코드

DOI QR Code

Bacteriophage Usage for Bacterial Disease Management and Diagnosis in Plants

  • Vu, Nguyen Trung (Department of Horticultural Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Oh, Chang-Sik (Department of Horticultural Biotechnology, College of Life Sciences, Kyung Hee University)
  • Received : 2020.04.22
  • Accepted : 2020.05.13
  • Published : 2020.06.01

Abstract

In nature, plants are always under the threat of pests and diseases. Pathogenic bacteria are one of the major pathogen types to cause diseases in diverse plants, resulting in negative effects on plant growth and crop yield. Chemical bactericides and antibiotics have been used as major approaches for controlling bacterial plant diseases in the field or greenhouse. However, the appearance of resistant bacteria to common antibiotics and bactericides as well as their potential negative effects on environment and human health demands bacteriologists to develop alternative control agents. Bacteriophages, the viruses that can infect and kill only target bacteria very specifically, have been demonstrated as potential agents, which may have no negative effects on environment and human health. Many bacteriophages have been isolated against diverse plant-pathogenic bacteria, and many studies have shown to efficiently manage the disease development in both controlled and open conditions such as greenhouse and field. Moreover, the specificity of bacteriophages to certain bacterial species has been applied to develop detection tools for the diagnosis of plant-pathogenic bacteria. In this paper, we summarize the promising results from greenhouse or field experiments with bacteriophages to manage diseases caused by plant-pathogenic bacteria. In addition, we summarize the usage of bacteriophages for the specific detection of plant-pathogenic bacteria.

Keywords

References

  1. Abedon, S. T., Kuhl, S. J., Blasdel, B. G. and Kutter, E. M. 2011. Phage treatment of human infections. Bacteriophage 1:66-85. https://doi.org/10.4161/bact.1.2.15845
  2. Addy, H. S., Askora, A., Kawasaki, T., Fujie, M. and Yamada, T. 2012. Utilization of filamentous phage ${\varphi}RSM3$ to control bacterial wilt caused by Ralstonia solanacearum. Plant Dis. 96:1204-1209. https://doi.org/10.1094/PDIS-12-11-1023-RE
  3. Adriaenssens, E. M., Van Vaerenbergh, J., Vandenheuvel, D., Dunon, V., Ceyssens, P.-J., De Proft, M., Kropinski, A. M., Noben, J.-P., Maes, M. and Lavigne, R. 2012. T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by 'Dickeya solani'. PLoS ONE 7:e33227. https://doi.org/10.1371/journal.pone.0033227
  4. Agrios, G. 2005. Plant pathology. 5th ed. Elsevier Academic Press, Burlington, MA, USA. 952 pp.
  5. Ahern, S. J., Das, M., Bhowmick, T. S., Young, R. and Gonzalez, C. F. 2014. Characterization of novel virulent broad-hostrange phages of Xylella fastidiosa and Xanthomonas. J. Bacteriol. 196:459-471. https://doi.org/10.1128/JB.01080-13
  6. Ahmad, A. A., Askora, A., Kawasaki, T., Fujie, M. and Yamada, T. 2014. The filamentous phage XacF1 causes loss of virulence in Xanthomonas axonopodis pv. citri, the causative agent of citrus canker disease. Front. Microbiol. 5:321.
  7. Arthurs, S. P., Lacey, L. A. and Behle, R. W. 2006. Evaluation of spray-dried lignin-based formulations and adjuvants as solar protectants for the granulovirus of the codling moth, Cydia pomonella (L). J. Invertebr. Pathol. 93:88-95. https://doi.org/10.1016/j.jip.2006.04.008
  8. Attai, H., Rimbey, J., Smith, G. P. and Brown, P. J. B. 2017. Expression of a peptidoglycan hydrolase from lytic bacteriophages Atu_ph02 and Atu_ph03 triggers lysis of Agrobacterium tumefaciens. Appl. Environ. Microbiol. 83:e01498-17.
  9. Bae, J. Y., Wu, J., Lee, H. J., Jo, E. J., Murugaiyan, S., Chung, E. and Lee, S.-W. 2012. Biocontrol potential of a lytic bacteriophage PE204 against bacterial wilt of tomato. J. Microbiol. Biotechnol. 22:1613-1620. https://doi.org/10.4014/jmb.1208.08072
  10. Balogh, B. 2002. Strategies for improving the efficacy of bacteriophages for controlling bacterial spot of tomato. M.S. thesis. University of Florida, Gainesville, FL, USA.
  11. Balogh, B. 2006. Characterization and use of bacteriophages associated with citrus bacterial pathogens for disease control. Ph.D. thesis. University of Florida, Gainesville, FL, USA.
  12. Balogh, B., Jones, J. B., Iriarte, F. B. and Momol, M. T. 2010. Phage therapy for plant disease control. Curr. Pharm. Biotechnol. 11:48-57. https://doi.org/10.2174/138920110790725302
  13. Balogh, B., Jones, J. B., Momol, M. T., Olson, S. M., Obradovic, A., King, P. and Jackson, L. E. 2003. Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis. 87:949-954. https://doi.org/10.1094/PDIS.2003.87.8.949
  14. Behlau, F., Canteros, B. I., Minsavage, G. V., Jones, J. B. and Graham, J. H. 2011. Molecular characterization of copper resistance genes from Xanthomonas citri subsp. citri and Xanthomonas alfalfae subsp. citrumelonis. Appl. Environ. Microbiol. 77:4089-4096. https://doi.org/10.1128/AEM.03043-10
  15. Behle, R. W., McGuire, M. R. and Shasha, B. S. 1996. Extending the residual toxicity of Bacillus thuringiensis with caseinbased formulations. J. Econ. Entomol. 89:1399-1405. https://doi.org/10.1093/jee/89.6.1399
  16. Bhunchoth, A., Phironrit, N., Leksomboon, C., Chatchawankanphanich, O., Kotera, S., Narulita, E., Kawasaki, T., Fujie, M. and Yamada, T. 2015. Isolation of Ralstonia solanacearuminfecting bacteriophages from tomato fields in Chiang Mai, Thailand, and their experimental use as biocontrol agents. J. Appl. Microbiol. 118:1023-1033. https://doi.org/10.1111/jam.12763
  17. Born, Y., Fieseler, L., Klumpp, J., Eugster, M. R., Zurfluh, K., Duffy, B. and Loessner, M. J. 2014. The tail-associated depolymerase of Erwinia amylovora phage L1 mediates host cell adsorption and enzymatic capsule removal, which can enhance infection by other phage. Environ. Microbiol. 16:2168-2180. https://doi.org/10.1111/1462-2920.12212
  18. Born, Y., Fieseler, L., Thony, V., Leimer, N., Duffy, B. and Loessner, M. J. 2017. Engineering of bacteriophages Y2::dpoL1-C and Y2::luxAB for efficient control and rapid detection of the fire blight pathogen, Erwinia amylovora. Appl. Environ. Microbiol. 83:e00341-17.
  19. Borysowski, J., Weber-Dabrowska, B. and Gorski, A. 2006. Bacteriophage endolysins as a novel class of antibacterial agents. Exp. Biol. Med. (Maywood) 231:366-377. https://doi.org/10.1177/153537020623100402
  20. Boule, J., Sholberg, P. L., Lehman, S. M., O'gorman, D. T. and Svircev, A. M. 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. 33:308-317. https://doi.org/10.1080/07060661.2011.588250
  21. Boyd, R. J., Hildebrandt, A. C. and Allen, O. N. 1971. Retardation of crown gall enlargement after bacteriophage treatment. Plant Dis. Rep. 55:145-148.
  22. Burnham, S., Hu, J., Anany, H., Brovko, L., Deiss, F., Derda, R. and Griffiths, M. W. 2014. Towards rapid on-site phagemediated detection of generic Escherichia coli in water using luminescent and visual readout. Anal. Bioanal. Chem. 406:5685-5693. https://doi.org/10.1007/s00216-014-7985-3
  23. Buttimer, C., McAuliffe, O., Ross, R. P., Hill, C., O'Mahony, J. and Coffey, A. 2017. Bacteriophages and bacterial plant diseases. Front. Microbiol. 8:34.
  24. Calvo-Garrido, C., Vinas, I., Elmer, P. A., Usall, J. and Teixido, N. 2014. Suppression of Botrytis cinerea on necrotic grapevine tissues by early-season applications of natural products and biological control agents. Pest Manag. Sci. 70:595-602. https://doi.org/10.1002/ps.3587
  25. Carisse, O., Philion, V., Rolland, D. and Bernier, J. 2000. Effect of fall application of fungal antagonists on spring ascospore production of the apple scab pathogen, Venturia inaequalis. Phytopathology 90:31-37. https://doi.org/10.1094/PHYTO.2000.90.1.31
  26. Chae, J.-C., Hung, N. B., Yu, S.-M., Lee, H. K. and Lee, Y. H. 2014. Diversity of bacteriophages infecting Xanthomonas oryzae pv. oryzae in paddy fields and its potential to control bacterial leaf blight of rice. J. Microbiol. Biotechnol. 24:740-747. https://doi.org/10.4014/jmb.1402.02013
  27. Chopin, M.-C., Chopin, A. and Bidnenko, E. 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473-479. https://doi.org/10.1016/j.mib.2005.06.006
  28. Civerolo, E. L. 1973. Relationship of Xanthomonas pruni bacteriophages to bacterial spot disease in prunus. Phytopathology 63:1279-1284. https://doi.org/10.1094/Phyto-63-1279
  29. Civerolo, E. L. and Keil, H. L. 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59:1966-1967.
  30. Coffey, A. and Ross, R. P. 2002. Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie Van Leeuwenhoek 82: 303-321. https://doi.org/10.1023/A:1020639717181
  31. Compant, S., Duffy, B., Nowak, J., Clement, C. and Barka, E. A. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71:4951-4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005
  32. Coons, G. H. and Kotila, J. E. 1925. The transmissible lytic principle (bacteriophage) in relation to plant pathogens. Phytopathology 15:357-370.
  33. Davies, E. V., Winstanley, C., Fothergill, J. L. and James, C. E. 2016. The role of temperate bacteriophages in bacterial infection. FEMS Microbiol. Lett. 363:fnw015. https://doi.org/10.1093/femsle/fnw015
  34. Dennis, C. and Webster, J. 1971. Antagonistic properties of species-groups of Trichoderma: I. Production of non-volatile antibiotics. Trans. Br. Mycol. Soc. 57:25-39. https://doi.org/10.1016/s0007-1536(71)80077-3
  35. d'Herelle, F. 1917. Sur un microbe invisible antagoniste des Bacillies dysenterique. C. R. Acad. Sci. 165:373-375.
  36. Dong, S., Shew, H. D., Tredway, L. P., Lu, J., Sivamani, E., Miller, E. S. and Qu, R. 2008. Expression of the bacteriophage T4 lysozyme gene in tall fescue confers resistance to gray leaf spot and brown patch diseases. Transgenic Res. 17:47-57. https://doi.org/10.1007/s11248-007-9073-3
  37. Dong, Z., Xing, S., Liu, J., Tang, X., Ruan, L., Sun, M., Tong, Y. and Peng, D. 2018. Isolation and characterization of a novel phage Xoo-sp2 that infects Xanthomonas oryzae pv. oryzae. J. Gen. Virol. 99:1453-1462. https://doi.org/10.1099/jgv.0.001133
  38. Drulis-Kawa, Z., Majkowska-Skrobek, G. and Maciejewska, B. 2015. Bacteriophages and phage-derived proteins: application approaches. Curr. Med. Chem. 22:1757-1773. https://doi.org/10.2174/0929867322666150209152851
  39. Dy, R. L., Rigano, L. A. and Fineran, P. C. 2018. Phage-based biocontrol strategies and their application in agriculture and aquaculture. Biochem. Soc. Trans. 46:1605-1613. https://doi.org/10.1042/BST20180178
  40. Elhalag, K., Nasr-Eldin, M., Hussien, A. and Ahmad, A. 2018. Potential use of soilborne lytic Podoviridae phage as a biocontrol agent against Ralstonia solanacearum. J. Basic Microbiol. 58:658-669. https://doi.org/10.1002/jobm.201800039
  41. Farooq, U., Yang, Q., Ullah, M. W. and Wang, S. 2018. Bacterial biosensing: recent advances in phage-based bioassays and biosensors. Biosens. Bioelectron. 118:204-216. https://doi.org/10.1016/j.bios.2018.07.058
  42. Flaherty, J. E., Harbaugh, B. K., Jones, J. B., Somodi, G. C. and Jackson, L. E. 2001. H-mutant bacteriophages as a potential biocontrol of bacterial blight of geranium. HortScience 36:98-100. https://doi.org/10.21273/hortsci.36.1.98
  43. Flaherty, J. E., Jones, J. B., Harbaugh, B. K., Somodi, G. C. and Jackson, L. E. 2000. Control of bacterial spot on tomato in the greenhouse and field with H-mutant bacteriophages. HortScience 35:882-884. https://doi.org/10.21273/hortsci.35.5.882
  44. Flockhart, A. F., Tree, J. J., Xu, X., Karpiyevich, M., McAteer, S. P., Rosenblum, R., Shaw, D. J., Low, C. J., Best, A., Gannon, V., Laing, C., Murphy, K. C., Leong, J. M., Schneiders, T., La Ragione, R. and Gally, D. L. 2012. Identification of a novel prophage regulator in Escherichia coli controlling the expression of type III secretion. Mol. Microbiol. 83:208-223. https://doi.org/10.1111/j.1365-2958.2011.07927.x
  45. Forde, A., Daly, C. and Fitzgerald, G. F. 1999. Identification of four phage resistance plasmids from Lactococcus lactis subsp. cremoris $HO_2$. Appl. Environ. Microbiol. 65:1540-1547. https://doi.org/10.1128/aem.65.4.1540-1547.1999
  46. Fortier, L.-C. and Sekulovic, O. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354-365. https://doi.org/10.4161/viru.24498
  47. Frampton, R. A., Taylor, C., Moreno, A. V. H., Visnovsky, S. B., Petty, N. K., Pitman, A. R. and Fineran, P. C. 2014. Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Appl. Environ. Microbiol. 80:2216-2228. https://doi.org/10.1128/AEM.00062-14
  48. Frobisher, M. Jr. and Brown, J. H. 1927. Transmissible toxicogenicity of streptococci. Bull. Johns Hopkins Hosp. 41:167-173.
  49. Fujiwara, A., Fujisawa, M., Hamasaki, R., Kawasaki, T., Fujie, M. and Yamada, T. 2011. Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Appl. Environ. Microbiol. 77:4155-4162. https://doi.org/10.1128/AEM.02847-10
  50. Gasic, K., Kuzmanovic, N., Ivanovic, M., Prokic, A., Sevic, M. and Obradovic, A. 2018. Complete genome of the Xanthomonas euvesicatoria specific bacteriophage $K{\Phi}1$, its survival and potential in control of pepper bacterial spot. Front. Microbiol. 9:2021. https://doi.org/10.3389/fmicb.2018.02021
  51. Gill, J. and Abedon, S. T. 2003. Bacteriophage ecology and plants. APSnet Features. https://doi.org/10.1094/APSnetFeature-2003-1103.
  52. Gomez, P. and Buckling, A. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106-109. https://doi.org/10.1126/science.1198767
  53. Goto, M. 2012. Fundamentals of bacterial plant pathology. Academic Press, Burlington, MA, USA. 342 pp.
  54. Greer, G. G. 2005. Bacteriophage control of foodborne bacteria. J. Food Prot. 68:1102-1111. https://doi.org/10.4315/0362-028X-68.5.1102
  55. Groman, N. B. 1953. Evidence for the induced nature of the change from nontoxigenicity to toxigenicity in Corynebacterium diphtheriae as a result of exposure to specific bacteriophage. J. Bacteriol. 66:184-191. https://doi.org/10.1128/jb.66.2.184-191.1953
  56. Groman, N. B. 1955. Evidence for the active role of bacteriophage in the conversion of nontoxigenic Corynebacterium diphtheriae to toxin production. J. Bacteriol. 69:9-15. https://doi.org/10.1128/jb.69.1.9-15.1955
  57. Hagens, S. and Loessner, M. J. 2007. Application of bacteriophages for detection and control of foodborne pathogens. Appl. Microbiol. Biotechnol. 76:513-519. https://doi.org/10.1007/s00253-007-1031-8
  58. Hermoso, J. A., Garcia, J. L. and Garcia, P. 2007. Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr. Opin. Microbiol. 10:461-472. https://doi.org/10.1016/j.mib.2007.08.002
  59. Howard-Varona, C., Hargreaves, K. R., Abedon, S. T. and Sullivan, M. B. 2017. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J. 11:1511-1520. https://doi.org/10.1038/ismej.2017.16
  60. Hwang, M. S., Morgan, R. L., Sarkar, S. F., Wang, P. W. and Guttman, D. S. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 71:5182-5191. https://doi.org/10.1128/AEM.71.9.5182-5191.2005
  61. Ibrahim, Y. E., Saleh, A. A. and Al-Saleh, M. A. 2017. Management of asiatic citrus canker under field conditions in Saudi Arabia using bacteriophages and acibenzolar-S-methyl. Plant Dis. 101:761-765. https://doi.org/10.1094/PDIS-08-16-1213-RE
  62. Ignoffo, C. M., Garcia, C. and Saathoff, S. G. 1997. Sunlight stability and rain-fastness of formulations of Baculovirus heliothis. Environ. Entomol. 26:1470-1474. https://doi.org/10.1093/ee/26.6.1470
  63. Iriarte, F. B., Balogh, B., Momol, M. T., Smith, L. M., Wilson, M. and Jones, J. B. 2007. Factors affecting survival of bacteriophage on tomato leaf surfaces. Appl. Environ. Microbiol. 73:1704-1711. https://doi.org/10.1128/AEM.02118-06
  64. Javed, M. A., Poshtiban, S., Arutyunov, D., Evoy, S. and Szymanski, C. M. 2013. Bacteriophage receptor binding protein based assays for the simultaneous detection of Campylobacter jejuni and Campylobacter coli. PLoS ONE 8:e69770. https://doi.org/10.1371/journal.pone.0069770
  65. Koskella, B. and Brockhurst, M. A. 2014. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38:916-931. https://doi.org/10.1111/1574-6976.12072
  66. Kotila, J. E. and Coons, G. H. 1925. Investigations on the blackleg disease of the potato. Mich. Agric. Exp. Stn. Tech. Bull. 67:3-29.
  67. Kuo, T. T., Chang, L. C., Yang, C. M. and Yang, S. E. 1971. Bacterial leaf blight of rice plant. IV. Effect of bacteriophage on the infectivity of Xanthomonas oryzae. Acad. Sin. Inst. Bot. Bot. Bull. 12:1-9.
  68. Kutin, R. K., Alvarez, A. and Jenkins, D. M. 2009. Detection of Ralstonia solanacearum in natural substrates using phage amplification integrated with real-time PCR assay. J. Microbiol. Methods 76:241-246. https://doi.org/10.1016/j.mimet.2008.11.008
  69. Lai, M.-J., Soo, P.-C., Lin, N.-T., Hu, A., Chen, Y.-J., Chen, L.-K. and Chang, K.-C. 2013. Identification and characterisation of the putative phage-related endolysins through full genome sequence analysis in Acinetobacter baumannii ATCC 17978. Int. J. Antimicrob. Agents 42:141-148. https://doi.org/10.1016/j.ijantimicag.2013.04.022
  70. Lang, J. M., Gent, D. H. and Schwartz, H. F. 2007. Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis. 91:871-878. https://doi.org/10.1094/PDIS-91-7-0871
  71. Le Roy, E. J. 1989. Bacteriophage prevention and control of harmful plant bacteria. U.S. Patent No. US4828999A. U.S. Patent and Trademark Office, Washington, DC, USA.
  72. Lee, Y. A., Hendson, M., Panopoulos, N. J. and Schroth, M. N. 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. https://doi.org/10.1128/jb.176.1.173-188.1994
  73. Leverentz, B., Conway, W. S., Camp, M. J., Janisiewicz, W. J., Abuladze, T., Yang, M., Saftner, R. and Sulakvelidze, A. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69:4519-4526. https://doi.org/10.1128/AEM.69.8.4519-4526.2003
  74. Lim, J.-A., Jee, S., Lee, D. H., Roh, E., Jung, K., Oh, C. and Heu, S. 2013. Biocontrol of Pectobacterium carotovorum subsp. carotovorum using bacteriophage PP1. J. Microbiol. Biotechnol. 23:1147-1153. https://doi.org/10.4014/jmb.1304.04001
  75. Loc-Carrillo, C. and Abedon, S. T. 2011. Pros and cons of phage therapy. Bacteriophage 1:111-114. https://doi.org/10.4161/bact.1.2.14590
  76. Lood, R., Winer, B. Y., Pelzek, A. J., Diez-Martinez, R., Thandar, M., Euler, C. W., Schuch, R. and Fischetti, V. A. 2015. Novel phage lysin capable of killing the multidrug-resistant gramnegative bacterium Acinetobacter baumannii in a mouse bacteremia model. Antimicrob. Agents Chemother. 59:1983-1991. https://doi.org/10.1128/AAC.04641-14
  77. Mallmann, W. L. and Hemstreet, C. 1924. Isolation of an inhibitory substance from plants. J. Agric. Res. 28:599-602.
  78. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G. and Foster, G. D. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614-629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
  79. Manulis, S., Kleitman, F., Dror, O. and Shabi, E. 2000. Isolation of strains of Erwinia amylovora resistant to oxolinic acid. IOBC/WPRS Bull. 23:89-92.
  80. Masami, N., Masao, G., Katsumi, A. and Tadaaki, H. 2004. Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. actinidiae. Eur. J. Plant Pathol. 110:223-226. https://doi.org/10.1023/b:ejpp.0000015360.88352.a9
  81. McManus, P. S., Stockwell, V. O., Sundin, G. W. and Jones, A. L. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-465. https://doi.org/10.1146/annurev.phyto.40.120301.093927
  82. Mellano, M. A. and Cooksey, D. A. 1988. Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. tomato. J. Bacteriol. 170:2879-2883. https://doi.org/10.1128/jb.170.6.2879-2883.1988
  83. Morgan, A. D., Bonsall, M. B. and Buckling, A. 2010. Impact of bacterial mutation rate on coevolutionary dynamics between bacteria and phages. Evolution 64:2980-2987.
  84. Nagai, H., Miyake, N., Kato, S., Maekawa, D., Inoue, Y. and Takikawa, Y. 2017. Improved control of black rot of broccoli caused by Xanthomonas campestris pv. campestris using a bacteriophage and a nonpathogenic Xanthomonas sp. strain. J. Gen. Plant Pathol. 83:373-381. https://doi.org/10.1007/s10327-017-0745-4
  85. Nanda, A. M., Thormann, K. and Frunzke, J. 2015. Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions. J. Bacteriol. 197:410-419. https://doi.org/10.1128/JB.02230-14
  86. Nelson, D. C., Schmelcher, M., Rodriguez-Rubio, L., Klumpp, J., Pritchard, D. G., Dong, S. and Donovan, D. M. 2012. Endolysins as antimicrobials. Adv. Virus Res. 83:299-365. https://doi.org/10.1016/B978-0-12-394438-2.00007-4
  87. Obradovic, A., Jones, J. B., Momol, M. T., Olson, S. M., Jackson, L. E., Balogh, B., Guven, K. and Iriarte, F. B. 2005. Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis. 89:712-716. https://doi.org/10.1094/PD-89-0712
  88. Okabe, N. and Goto, M. 1963. Bacteriophages of plant pathogens. Annu. Rev. Phytopathol. 1:397-418. https://doi.org/10.1146/annurev.py.01.090163.002145
  89. Pohane, A. A. and Jain, V. 2015. Insights into the regulation of bacteriophage endolysin: multiple means to the same end. Microbiology 161:2269-2276. https://doi.org/10.1099/mic.0.000190
  90. Rahimi-Midani, A., Lee, Y. S., Kang, S.-W., Kim, M.-K. and Choi, T.-J. 2018. First isolation and molecular characterization of bacteriophages infecting Acidovorax citrulli, the causal agent of bacterial fruit blotch. Plant Pathol. J. 34:59-64. https://doi.org/10.5423/PPJ.NT.08.2017.0190
  91. Ramirez, M., Neuman, B. and Ramirez, C. A. 2020. Bacteriophages as promising agents for the biological control of moko disease (Ralstonia solanacearum) of banana. Biol. Control. (in press). https://doi.org/10.1016/j.biocontrol.2020.104238.
  92. Ranjani, P., Gowthami, Y., Gnanamanickam, S. S. and Palani, P. 2018. Bacteriophages: a new weapon for the control of bacterial blight disease in rice caused by Xanthomonas oryzae. Microbiol. Biotechnol. Lett. 46:346-359. https://doi.org/10.4014/mbl.1807.07009
  93. Rezzonico, F., Smits, T. H. and Duffy, B. 2011. Diversity, evolution, and functionality of clustered regularly interspaced short palindromic repeat (CRISPR) regions in the fire blight pathogen Erwinia amylovora. Appl. Environ. Microbiol. 77:3819-3829. https://doi.org/10.1128/AEM.00177-11
  94. Rombouts, S., Volckaert, A., Venneman, S., Declercq, B., Vandenheuvel, D., Allonsius, C. N., Van Malderghem, C., Jang, H. B., Briers, Y., Noben, J. P., Klumpp, J., Van Vaerenbergh, J., Maes, M. and Lavigne, R. 2016. Characterization of novel bacteriophages for biocontrol of bacterial blight in leek caused by Pseudomonas syringae pv. porri. Front. Microbiol. 7:279.
  95. Russel, M., Linderoth, N. A. and Sali, A. 1997. Filamentous phage assembly: variation on a protein export theme. Gene 192:23-32. https://doi.org/10.1016/S0378-1119(96)00801-3
  96. Saccardi, A., Gambin, E., Zaccardelli, M., Barone, G. and Mazzucchi, U. 1993. Xanthomonas campestris pv. pruni control trials with phage treatments on peaches in the orchard. Phytopathol. Mediterr. 32:206-210.
  97. Santos, S. B., Costa, A. R., Carvalho, C., Nobrega, F. L. and Azeredo, J. 2018. Exploiting bacteriophage proteomes: the hidden biotechnological potential. Trends Biotechnol. 36:966-984. https://doi.org/10.1016/j.tibtech.2018.04.006
  98. Schmerer, M., Molineux, I. J. and Bull, J. J. 2014. Synergy as a rationale for phage therapy using phage cocktails. PeerJ 2:e590. https://doi.org/10.7717/peerj.590
  99. Schnabel, E. L., Fernando, W. G. D., Meyer, M. P., Jones, A. L. and Jackson, L. E. 1998. Bacteriophage of Erwinia amylovora and their potential for biocontrol. Acta Hortic. 489:649-654. https://doi.org/10.17660/actahortic.1999.489.116
  100. Schofield, D. A., Bull, C. T., Rubio, I., Wechter, W. P., Westwater, C. and Molineux, I. J. 2013. "Light-tagged" bacteriophage as a diagnostic tool for the detection of phytopathogens. Bioengineered 4:50-54. https://doi.org/10.4161/bioe.22159
  101. Semenova, E., Nagornykh, M., Pyatnitskiy, M., Artamonova, I. I. and Severinov, K. 2009. Analysis of CRISPR system function in plant pathogen Xanthomonas oryzae. FEMS Microbiol. Lett. 296:110-116. https://doi.org/10.1111/j.1574-6968.2009.01626.x
  102. Singh, A., Arutyunov, D., Szymanski, C. M. and Evoy, S. 2012. Bacteriophage based probes for pathogen detection. Analyst 137:3405-3421. https://doi.org/10.1039/c2an35371g
  103. Stall, R. E. 1962. Streptomycin resistance of the bacterial spot pathogen and control with streptomycin. Plant Dis. Rep. 46:389-392.
  104. Stonier, T., McSharry, J. and Speitel, T. 1967. Agrobacterium tumefaciens Conn IV. Bacteriophage PB21 and its inhibitory effect on tumor induction. J. Virol. 1:268-273. https://doi.org/10.1128/jvi.1.2.268-273.1967
  105. Sulakvelidze, A., Alavidze, Z. and Morris, J. G. Jr. 2001. Bacteriophage therapy. Antimicrob. Agent Chemother. 45:649-659. https://doi.org/10.1128/AAC.45.3.649-659.2001
  106. Sutton, M. D. and Katznelson, H. 1953. Isolation of bacteriophages for the detection and identification of some seedborne pathogenic bacteria. Can. J. Bot. 31:201-205. https://doi.org/10.1139/b53-019
  107. Svircev, A., Roach, D. and Castle, A. 2018. Framing the future with bacteriophages in agriculture. Viruses 10:E218.
  108. Tanaka, H., Negishi, H. and 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. https://doi.org/10.3186/jjphytopath.56.243
  109. Tewfike, T. A. and Desoky, S. M. 2015. Biocontrol of Xanthomonas axonopodis causing bacterial spot by application of formulated phage. Ann. Agric. Sci. Moshtohor. 53:615-624. https://doi.org/10.21608/assjm.2015.109939
  110. Thomas, R. 1935. A bacteriophage in relation to Stewart's disease of corn. Phytopathology 25:371-372.
  111. Twort, F. W. 1915. An Investigation on the nature of ultra-microscopic viruses. Lancet 186:1241-1243. https://doi.org/10.1016/S0140-6736(01)20383-3
  112. Wang, X., Wei, Z., Yang, K., Wang, J., Jousset, A., Xu, Y., Shen, Q. and Friman, V.-P. 2019. Phage combination therapies for bacterial wilt disease in tomato. Nat. Biotechnol. 37:1513-1520. https://doi.org/10.1038/s41587-019-0328-3
  113. Weber-Dabrowska, B., Mulczyk, M. and Gorski, A. 2001. Bacteriophage therapy for infections in cancer patients. Clin. Appl. Immunol. Rev. 1:131-134. https://doi.org/10.1016/S1529-1049(01)00015-0
  114. Wei, C., Liu, J., Maina, A. N., Mwaura, F. B., Yu, J., Yan, C., Zhang, R. and Wei, H. 2017. Developing a bacteriophage cocktail for biocontrol of potato bacterial wilt. Virol. Sin. 32:476-484. https://doi.org/10.1007/s12250-017-3987-6
  115. Weinbauer, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181. https://doi.org/10.1016/j.femsre.2003.08.001
  116. Weng, S.-F., Fu, Y.-C., Lin, J.-W. and Tseng, T.-T. 2018. Identification of a broad-spectrum peptidoglycan hydrolase associated with the particle of Xanthomonas oryzae phage Xop411. J. Mol. Microbiol. Biotechnol. 28:78-86. https://doi.org/10.1159/000488678
  117. Wiesel, L., Newton, A. C., Elliott, I., Booty, D., Gilroy, E. M., Birch, P. R. J. and Hein, I. 2014. Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front. Plant Sci. 5:655.
  118. Wilhelm, S. W. and Suttle, C. A. 1999. Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49:781-788. https://doi.org/10.2307/1313569
  119. Wittmann, J., Brancato, C., Berendzen, K. W. and Dreiseikelmann, B. 2016. Development of a tomato plant resistant to Clavibacter michiganensis using the endolysin gene of bacteriophage CMP1 as a transgene. Plant Pathol. 65:496-502. https://doi.org/10.1111/ppa.12417
  120. Wittmann, J., Eichenlaub, R. and Dreiseikelmann, B. 2010. The endolysins of bacteriophages CMP1 and CN77 are specific for the lysis of Clavibacter michiganensis strains. Microbiology 156:2366-2373. https://doi.org/10.1099/mic.0.037291-0
  121. Yin, Y., Ni, P., Deng, B., Wang, S., Xu, W. and Wang, D. 2019. Isolation and characterisation of phages against Pseudomonas syringae pv. actinidiae. Acta. Agric. Sect. B Soil Plant Sci. 69:199-208.
  122. Yu, J.-G., Lim, J.-A., Song, Y.-R., Heu, S., Kim, G. H., Koh, Y. J. and Oh, C.-S. 2016. Isolation and characterization of bacteriophages against Pseudomonas syringae pv. actinidiae causing bacterial canker disease in kiwifruit. J. Microbiol. Biotechnol. 26:385-393. https://doi.org/10.4014/jmb.1509.09012
  123. Zaczek-Moczydlowska, M. A., Young, G. K., Trudgett, J., Fleming, C. C., Campbell, K. and O'Hanlon, R. 2020. Genomic characterization, formulation and efficacy in planta of a Siphoviridae and Podoviridae protection cocktail against the bacterial plant pathogens Pectobacterium spp. Viruses 12:150. https://doi.org/10.3390/v12020150