The Future of Phage-Mediated Biocontrol of Tomato Bacterial Diseases

Abstract

Phytopathogenic bacteria cause significant economic losses in tomato production. Tomato bacterial spot, speck, wilt and cancer disease agents are the most important phytopathogens that cause damage to tomatoes. Chemical methods have been generally used to control these diseases. However, the disadvantages of chemicals like development of resistance in bacterial strains, damage to non-target microorganisms and undesirable effects on the environment have increased the interest in alternative control strategies for sustainable agriculture. The use of bacteriophages, virus infecting bacteria, provides a remarkable alternative in controlling bacterial diseases of tomato. On the other hand, phage-mediated control strategies have three main limitations which are emergence of resistance in bacteria, stability during storage and persistence in the environment. The development of resistance can be mitigated or prevented using phage cocktails. In addition, encapsulation methods such as lyophilization (freeze-drying), emulsification and spray drying can be used for prolonging shelf life and increase the efficacy in field conditions. Studies on the use of phages against tomato bacterial diseases remained mostly as laboratory experiments, and except AgriPhage, a commercialized product, there is no product that can be used to treat diseases under field conditions. The use of eco-friendly products based on bacteriophages is very important for sustainable agriculture. This review compiled information on useful formulation of phage and phages identified in combating four tomato bacterial diseases which was determined as bacterial canker, bacterial speck, bacterial wilt and bacterial spot.

Keywords

• Phytopathogenic bacteria
• bacteriophage
• formulation
• biocontrol
• tomato diseases

Domates bakteriyel hastalıklarının faj aracılı biyokontrolünün geleceği

Abstract

Fitopatojenik bakteriler domates üretiminde önemli ekonomik kayıplara neden olmaktadır. Domates bakteriyel leke, benek, solgunluk ve kanser hastalığı etkenleri, domateslere zarar veren en önemli fitopatojenlerdir. Bu hastalıkları kontrol altına almak için genellikle kimyasal yöntemler kullanılmıştır. Ancak kimyasalların bakteri suşlarında direnç geliştirmesi, hedef olmayan mikroorganizmalara verdiği zararlar ve çevre üzerindeki istenmeyen etkileri gibi dezavantajları, sürdürülebilir tarım için alternatif mücadele stratejilerine olan ilgiyi artırmıştır. Bakteriyofajların kullanımı, domatesi bakteriyel hastalıklarının kontrolünde dikkate değer bir alternatif sunmaktadır. Öte yandan, faj aracılı kontrol stratejilerinin, bakterilerde direncin ortaya çıkması, depolama sırasında stabilite ve çevrede kalıcılık olmak üzere üç ana sınırlaması vardır. Direnç gelişimi, faj kokteylleri kullanılarak hafifletilebilir veya önlenebilir. Ayrıca liyofilizasyon (dondurarak kurutma), emülsifikasyon ve sprey kurutma gibi enkapsülasyon yöntemleri de saha koşullarında raf ömrünü uzatmak ve etkinliği artırmak için kullanılabilir. Fajların domates bakteriyel hastalıklarına karşı kullanımı ile ilgili çalışmalar daha çok laboratuvar deneyleri olarak kalmış ve ticarileştirilmiş bir ürün olan Agriphage dışında tarla koşullarında hastalıkları tedavi etmek için kullanılabilecek bir ürün bulunmamaktadır. Sürdürülebilir tarım için bakteriyofaj bazlı çevre dostu ürünlerin kullanımı oldukça önemlidir. Bu derlemede bakteriyel kanser, bakteriyel benek, bakteriyel solgunluk ve bakteriyel leke olarak belirlenen dört domates bakteriyel hastalığıyla mücadelede tanımlanan faj ve fajların faydalı formülasyonu hakkında bilgiler derlenmiştir.

Keywords

• Fitopatojenik bakteriler
• bakteriyofaj
• formülasyon
• biyokontrol
• domates hastalıkları

References

1. FAO (2021) FAOSTAT. Available Online: https://www.fao.org/faostat/en/#data/QC/visualize Accessed 25 January 2022.
2. S. Elnaggar, A.M. Mohamed, A. Bakeer and T.A. Osman, “Current Status of Bacterial Wilt (Ralstonia solanacearum) Disease in Major Tomato (Solanum lycopersicum L.) Growing Areas in Egypt”, Arch. Agric. Environ. Sci, vol. 3, pp. 399-406, 2018.
3. J.B. Jones, T.A. Zitter, T.M. Momol and S.A. Miller, “Compendium of Tomato Diseases and Pests. Minnesota: American Phytopathological Society Publications, 2014.
4. P.L. Thayer and R.E. Stall, “A Survey of Xanthomonas vesicatoria Resistance to Streptomycin”, Proc. Annu. Meet Fla. State Hort. Soc., vol. 75, pp. 163-165, 1961.
5. A.L. Torre, V. Lovino and F. Caradonia, “Copper in Plant Protection: Current Situation and Prospects”, Phytopathol. Mediterr, vol. 57, pp. 201−236, 2018.
6. A. Svircev, D. Roach and A. Castle, “Framing The Future with Bacteriophages in Agriculture”, Viruses, vol. 10, pp. 218, 2018.
7. B. Balogh, “Strategies for Improving The Efficacy of Bacteriophages for Controlling Bacterial Spot of Tomato”, Dissertation, University of Florida, 2002.
8. E.F. Smith, “A New Tomato Disease of Economic Importance”, Science (New Series), vol. 31, pp. 794-796, 1910.

9. G.A. Shaker, “Identification of the Bacterium Tomato Stem Canker”, Am. J. Infect. Dis., vol. 10, pp. 44-49, 2014.
10. M.L. Gleason, E.J. Braun, W.M. Cariton and R.H. Peterson, “Survival and Dissemination of Clavibacter michiganensis subsp. michiganensis in Tomato”, Phytopathology, vol. 81, pp. 1519-23, 1991.
11. M.L. Gleason, R.D. Gitaitis and M.D.Ricker, “Recent Progress in Understanding and Controlling Bacterial Canker of Tomato in Eastern North America”, Plant Dis, vol. 77, pp. 1069- 76, 1993.
12. A. Kelman and J.H. Jensen, “Maintaining Virulence in Isolates of Pseudomonas solanacearum”, Phytopathology, vol. 41, pp. 185-187, 1951.
13. E.F. Smith, “The Brown Rot of Solanaceae. Bacterial Diseases of Plants”, U.S.A. Saunders Company, pp.177, 1920.
14. A. Kelman, “The Bacterial Wilt Caused by Pseudomonas solanacearum. A Literature Review and Bibliography”, Raleigh, N.C.: North Carolina State College, 1953.
15. N. Okabe, “Bacterial Diseases of Plants Occurring in Formosa: II. Bacterial Leaf Spot of Tomato”, J. Soc. Trop. Agric., vol. 5, pp. 26-36, 1933.
16. G.M. Preston, “Pseudomonas syringae pv. tomato: the Right Pathogen, of the Right Plant, at the Right Time”, Mol. Plant Pathol., vol. 1, pp. 263-275, 2000.
17. E.M. Doidge, “A Tomato Cankers”, Ann. Appl. Biol., vol. 7, pp. 407-430, 1921.
18. D. Šutic, “Bakterioze Crvenog Patlidzana [Tomato Bacteriosis]”, Posebna Izd Inst Zasht Bilja Beograd, vol. 6, pp. 1-65, 1957.
19. D.W. Dye, “Cultural and Biochemical Reaction of Additional Xanthomonas Spesies”, New Zeal. J. Sci., vol. 9, pp. 913-19, 1966.
20. J.M. Young,D.W. Dye, J.F. Bradbury, C.G. Panagopoulos and C.F.Robbs, “A Proposed Nomenclature and Classification for Plant Pathogenic Bacteria”, New Zeal. J. Agr. Res., vol. 21, pp. 153-177, 1978.
21. L. Vaulterin, B. Hoste, K. Kersters and J. Swings, “Reclassification of Xanthomonas”, Int. J. Syst. Evol, vol. 45, pp. 472-489, 1995.
22. J.B. Jones, G.H. Lacy, H. Bouzar, R.E. Stall and N.W. Schaad, “Reclassification of the Xanthomonads Associated with Bacterial Spot Disease of Tomato and Pepper”, Syst Appl Microbiol., vol. 27, pp. 755- 62, 2004.
23. J.D. Barak, T. Vancheva, P. Lefeuvre, J.B. Jones, S. Timilsina, G.V. Minsavage, G.E. Vallad and R. Koebnik, “Whole-Genome Sequences of Xanthomonas euvesicatoria Strains Clarify Taxonomy and Reveal a Stepwise Erosion of Type 3 Effectors”, Front Plant Sci., vol. 7, pp. 1805, 2016.
24. Z. Cui, M.R. Ojaghian, Z. Tao, K.U. Kakar, J. Zeng, W. Zhao, Y. Duan, C.M. Vera Cruz, B. Li, B. Zhu and G. Xie, “Multiplex PCR Assay for Simultaneous Detection of Six Major Bacterial Pathogens of Rice”, J. Appl. Microbiol. 2016; 120:1357-1367
25. J.B. Jones, G.H. Lacy, H. Bouzar, G.V. Minsavage, R.E. Stall, N.W. Schaad, “Bacterial Spot - Worldwide Distribution, Importance and Review”, Acta Horticult, vol. 695, pp. 27-36, 2005.
26. A.M. Kasselaki, D. Goumas, L. Tamm, , J. Fuchs, J. Cooper amd, C. Leifert, “Effect of Effective Strategies for the Disinfection of Tomato Seed Infected with Bacterial Canker (Clavibacter michiganensis subsp. michiganensis). NJAS-Wagen”, J. Life Sci., vol. 58, pp. 145-147, 2011.
27. P.M. Pradhanang and Colier, G. “How Effective is Hydrochloric Acid Treatment to Control Clavibacter michiganensis subsp. michiganensis Contamination in Tomato Seed”, Acta Hortic., vol. 808, pp. 81-85, 2009.
28. J.P. and Kumar, S. “Management of Ralstonia Wilt through Soil Disinfectant, Mulch, Lime and Cakes in Tomato (Lycopersicon esculentum)”, Indian J. Agric. Sci., vol. 70, pp. 17-19, 2000.
29. C.L. Bender and D.A. Cooksey, “Indigenous Plasmids in Pseudomonas syringae pv. tomato: Conjugative Transfer and Role on Copper Resistance”, J. Bacteriol. Res., vol. 165, pp. 534-541,1986.
30. C. Buttimer, O. McAuliffe, R.P. Ross, C. Hill, J. O’Mahony and A. Coffey, “Bacteriophages and Bacterial Plant Diseases”, Front. Microbiol. vol. 8, pp. 34, 2017.
31. Y.A. Nion and K. Toyota, “Recent Trends in Control Methods for Bacterial Wilt Diseases Caused by Ralstonia solanacearum”, Microbes Environ. pp.141-44, 2015.
32. F.M. Rhoads, S.M. Olson and A. Manning, “Copper Toxicity in Tomato Plants”, J. Environ. Qual., vol. 18, pp. 195-197, 1989.
33. S. Sonmez, M. Kaplan, K.N. Sonmez, H. Kaya and I. Uz, “High level of Copper Application to Soil and Leaves Reduce the Growth and Yield of Tomato Plants”, Sci. Agric., vol. 63, pp. 213-218, 2006.
34. J. Choi, K.H. Baek and E. Moon, “Antimicrobial Effects of a Hexapeptide KCM21 Against Pseudomonas syringae pv. tomato DC3000 and Clavibacter michiganensis subsp. michiganensis”, Plant Pathol. J., vol. 30, pp. 245-253, 2014.
35. J. Mercado-Blanco and P.A.H.M. Bakker, “Interactions between Plants and Beneficial Pseudomonas spp. Exploiting Bacterial Traits for Crop Protection”, Antonie Leeuwenhoek., vol. 92, pp. 367-389, 2007.
36. A.N. Babu, S. Jogaiah, S. Ito, A.K. Nagaraj and L.P. Tran, “Improvement of Growth, Fruit Weight and early Blight Disease Protection of Tomato Plants by Rhizosphere Bacteria is Correlated with Their Beneficial Traits and Induced Biosynthesis of Antioxidant Peroxidase and Polyphenol Oxidase”, Plant Sci., vol. 231, pp. 62-73, 2015.
37. I. Hammami, A.B. Hsouna, N. Hamdi, R. Gdoura and M.A. Triki, “Isolation and Characterization of Rhizosphere Bacteria for the Biocontrol of the Damping-off Disease of Tomatoes in Tunisia”, C. R. Biol., vol. 336, pp. 557-564, 2013.
38. P. Martinez-Hidalgo, J.M. Garcia and M.J Pozo, “Induced Systemic Resistance against Botrytis cinerea by Micromonospora Strains Isolated from Root Nodules”, Front. Microbiol., vol. 6, pp. 922, 2015.
39. N. Pastor, E. Carlier, J. Andrés, S.B. Rosas and M. Rovera, “Characterization of Rhizosphere Bacteria for Control of Phytopathogenic Fungi of Tomato”, J. Environ. Manage., vol. 95, pp. 33-337, 2012.
40. S. Umesha, “Occurrence of Bacterial Canker in Tomato Fields of Karnataka and Effect of Biological Seed Treatment on Disease Incidence”, J. Crop Prot., vol. 25, pp. 375-381, 2006.
41. A. Quattrucci, E. Ovidi, A. Tiezzi, V. Vinciguerra and G.M. Balestra, “Biological Control of Tomato Bacterial Speck Using Punica granatum Fruit Peel Extract”, Crop. Prot., vol. 46, pp. 18-22, 2012.
42. M.V. Arasu, N.A. Al-Dhabi, K.C. Choi, A.D.V. Bensy and J. Rajaselvam, “Bioactive Potential of Albizia lebbeck Extract against Phytopathogens and Protective Properties on Tomato Plant against Speck Disease in Greenhouse”, Physiol. Mol. Plant Pathol., vol. 117, pp. 101750, 2022.
43. M. Yılmaz, Ö. Baysal and R.S. Silme, The effect of a seed coating with Origanum vulgare Essential Oil on Clavibacter michiganensis subsp. michiganensis”, Plant Prot. Sci., vol. 57, pp. 217–225, 2021.
44. B. Balogh, J.B. Jones, F.B. Iriarte and M.T. Momol, “Phage therapy for plant disease control”, Curr. Pharm. Biotechnol., vol. 11, pp. 48–57, 2010.
45. N. Liu, C. Lewis, W. Zheng and Z.Q. Fu, “Phage cocktail therapy: multiple ways to suppress pathogenicity”, Trends Plant Sci., vol. 25, pp. 315-317, 2020.
46. S.T. Abedon, Phage ecology. In: R. Calender and S.T. Abedon (Eds.), The Bacteriophages (pp. 37-46). Oxford: Oxford University Press, 2006.
47. A. Campbell, “General Aspects of Lysogeny. in: R. Calender and S.T. Abedon (eds.), The Bacteriophages”, Oxford: Oxford University Press, pp. 66-73, 2006.
48. C. Howard-Varona, K.R. Hargreaves, S.T. Abedon and M.B. Sullivan, “Lysogeny in Nature Mechanisms, Impact and Ecology of Temperate Phages”, ISME, vol. 11, pp. 1511-1520, 2017.
49. I. Müller, R. Lurz and K. Geider, “Tasmancin and Lysogenic Bacteriophages Induced from Erwinia tasmaniensis Strains”, Microbiol. Res., vol. 167, pp. 381-387, 2012.
50. D. Holtappels, R. Lavigne, I. Huys and J. Wagemans, “Protection of Phage Applications in Crop Production: a Patent Landscape”, Viruses, vol. 11, pp. 1-16, 2019.
51. V.L. Taylor, A.D. Fitzpatrick, Z. Islam and K.L. Maxwell, “The Diverse Impacts of Phage Morons on Bacterial Fitness and Virulence”, Adv. Virus Res., vol. 103, pp. 1-31,2019.
52. P. Hyman and S.T. Abedon, “Bacteriophage Host Range and Bacterial Resistance”, Adv. Appl. Microbiol., vol. 70, pp. 217-248, 2010.
53. B. Koskella, D.M. Lin, A. Buckling and J.N. Thompson, The Costs of Evolving Resistance in Heterogeneous Parasite Environments”, Proc. Royal Soc., vol. 279, pp.1896-1903, 2012.
54. P.J. Looijesteijn, L. Trapet, E. de Vries, T. Abee and J. Hugenholtz, “Physiological Function of Exopolysaccharides Produced by Lactococcus lactis”, Int. J. Food Microbiol., vol. 64, pp. 71-80, 2001.
55. S.J. Labrie, J.E. Samson and S. Moineau, “Bacteriophage Resistance Mechanisms”, Nat. Rev. Microbiol., vol. 8, pp. 317-327, 2010.
56. J. Li, F. Zhao, W. Zhan, Z. Li, L. Zouc and Q. Zhaod, “Challenges for the Application of Bacteriophages as Effective Antibacterial Agents in the Food Industry”, J. Sci. Food Agric., vol. 102, pp. 461-471, 2020.
57. J.B. Jones, L.E. Jackson, B. Balogh, A. Obradovic, F.B. Iriarte and M.T. Momol, “Bacteriophages for Plant Disease Control”, Annu. Rev. Phytopathol., vol. 45, pp. 245-262, 2007.
58. M.D. Lang and K. Evans, “Epidemiology and Status of Walnut Blight in Australia”, J. Plant Pathol., vol. 92, pp. 49-55, 2010.
59. A. Ross, S. Ward and P. Hyman, “More is Better: Selecting for Broad Host Range Bacteriophages”, Front. Microbiol., vol. 7 pp. 1352, 2016.
60. F.I. Tovkach, “A Study of Erwinia carotovora Phage Resistance with the Use of Temperate Bacteriophage”, Microbiology, vol. 71, pp. 72-78, 2002.
61. J.E. Flatherty, J.B. Jones, B.K. Harbaugh, G.C. Somodi and L.E. Jackson, “Control of Bacterial Spot on Tomato in the Greenhouse and Field with H-Mutant Bacteriophages”, Hortscience, vol. 35, pp. 882- 884, 2000.
62. B. Balogh, J.B. Jones, M.T. Momol, S.M. Olson, A. Obradovic and P. King, “Improved Efficacy of Newly Formulated Bacteriophages for Management of Bacterial Spot on Tomato. Plant Dis., vol.87, pp. 949–54, 2003.
63. A. Fujiwara, M. Fujisawa, R. Hamasaki, T. Kawasaki, M. Fujie and T. Yamada, “Biocontrol of Ralstonia solanacearum by Treatment with Lytic Bacteriophages”, App. Environ. Microbiol., vol. 77, pp.4155-4162, 2011.
64. F.B. Iriarte, A. Obradovic, M.H. Wernsing, L.E. Jackson, B. Balogh, J.A. Hong, M.T. Momol, J.B. Jones and G.E. Vallad, “Soil-Based Systemic Delivery and Phyllosphere in vivo Propagation of Bacteriophages: Two Possible Strategies for Improving Bacteriophage Persistence for Plant Disease Control”, Bacteriophage, vol. 2, pp. 215-224, 2012.
65. D. Rosner and J. Clark, “Formulations for Bacteriophage Therapy and the Potential Uses of Immobilization”, Pharmaceuticals, vol. 14, pp.359, 2021.
66. D. Vandenheuvel, A. Singh, K. Vandersteegen, J. Klumpp, R. Lavigne, G. Van den Mooter, “Feasibility of Spray Drying Bacteriophages into Respirable Powders to Combat Pulmonary Bacterial Infections”, Eur. J. Pharm. Biopharm., vol. 84, pp. 578-582, 2013.
67. N.B. Carrigy, L. Liang, H. Wang, S. Kariuki, T.E. Nagel, I.F. Connerton and R. Vehring, “Trileucine and Pullulan Improve Anti-Campylobacter Bacteriophage Stability in Engineered Spray-Dried Microparticles”, Annu. Rev. Biomed. Eng., vol.48, pp.1169-1180, 2020.
68. S.S.Y. Leung, T. Parumasivam, F.G. Gao, E.A Carter, N.B. Carrigy, R. Vehring, W.H. Finlay, S. Morales, W.J. Britton and E. Kutter, “Effects of Storage Conditions on the Stability of Spray Dried Inhalable Bacteriophage Powders”, Int. J. Pharm., vol. 521, pp. 141-149, 2017.
69. J. Colom, M. Cano-Sarabia, J. Otero, P. Cortés, D. Maspoch and M. Llagostera, “Liposome Encapsulated Bacteriophages for Enhanced Oral Phage Therapy against Salmonella spp.”, Appl. Environ. Microbiol., vol. 81, pp.4841-4849, 2015.
70. H. Ackermann, D. Tremblay and S. Moineau, “Long-Term Bacteriophage Preservation”, WFCC Newsl., vol. 38, pp. 35-40, 2004.
71. U. Puapermpoonsiri, S.J. Ford and C.F. van der Walle, “Stabilization of Bacteriophage during Freeze Drying”, Int. J. Pharm., vol. 389, pp. 168-175, 2010.
72. B. Álvarez, L. Gadea-Pallás, A. Rodríguez, B. Vicedo, A. Figàs-Segura and E.G. Biosca, “Viability, stability and Biocontrol Activity in Planta of Specific Ralstonia solanacearum Bacteriophages after Their Conservation prior to Commercialization and Use”, Viruses, vol. 14, pp. 183, 2022.
73. OmniLytics., “Agriphage Product Info. Available at: https://www.agriphage.com/product-info/ “, 2006.
74. S. Murugaiyan, J.Y. Bae, J. Wu, S.D. Lee, H.Y. Um, H.K. Choi, E. Chung, H.L. Lee and S.W. Lee, “Characterization of Filamentous Bacteriophage PE226 Infecting Ralstonia solanacearum Strains”. J. Appl. Microbiol., vol. 110, pp. 296-30, 2010.
75. X. Wang, Z. Wei, K. Yang, J. Wang, A. Jousset, Y. Xu, Q, V.P. Shen Friman, “Phage Combination Therapies for Bacterial Wilt Disease in Tomato”, Nat. Biotechnol., vol. 37, pp. 1513-1520, 2019.
76. P.D. Umrao, V. Kumar and S.D. Kaistha “Biocontrol Potential of Bacteriophage ɸsp1 against Bacterial Wilt-Causing Ralstonia solanacearum in Solanaceae Crops”, Egypt. J. Biol. Pest Control, vol. 31, pp.1-12, 2021.
77. H.S. Addy, A. Askora, T. Kawasaki, M. Fujie and T. Yamada, “The Filamentous Phage Φrss1 Enhances Virulence of Phytopathogenic Ralstonia solanacearum on Tomato,” Phytopathology, vol.102, pp. 244-251, 2012.
78. K. Elhalag, M. Nasr‐Eldin, A. Hussien and A. Ahmad, “Potential use of Soilborne Lytic Podoviridae Phage as a Biocontrol Agent against Ralstonia solanacearum”, J. Basic Microbiol., vol. 58, pp.658-669, 2018.
79. A. Bhunchoth, N. Phironrit, C. Leksomboon, O. Chatchawankanphanich, S. Kotera, E. Narulita, T Kawasaki, M. Fujie and T. Yamada, “Isolation of Ralstonia solanacearum‐Infecting Bacteriophages From Tomato Fields in Chiang Mai, Thailand, and Their Experimental use as Biocontrol Agents”, J. Appl. Microbiol., vol.118, pp. 1023-1033, 2015.
80. M.D. Kalpage and D.M. De Costa, “Isolation of Bacteriophages and Determination of Their Efficiency in Controlling Ralstonia solanacearum Causing Bacterial Wilt of Tomato”, Tropical Agricultural Research vol. 26, pp. 140-151, 2014.
81. A. Obradovic, J.B. Jones, M.T. Momol, B., Balogh and S.M. Olson, “Management of Tomato Bacterial Spot in the Field by Foliar Applications of Bacteriophages and SAR Inducers”, Plant Dis., vol. 88, pp. 736-740, 2004.
82. K. Gašić, M.M. Ivanović, M. Ignjatov, A. Calić and A. Obradović, “Isolation and Characterization of Xanthomonas euvesicatoria Bacteriophages”, Plant Pathol., pp. 415-423, 2011.
83. Y. Kizheva, M. Eftimova, R. Rangelov, N. Micheva, Z. Urshev, I. Rasheva and P. Hristova, “Broad Host Range Bacteriophages Found in Rhizosphere Soil of a Healthy Tomato Plant in Bulgaria”, Heliyon, vol. 7, pp. 07084, 2021.
84. J. Wittmann, R. Eichenlaub and B. Dreiseikelmann, “The Endolysins of Bacteriophages CMP1 and CN77 are Specific for The Lysis of Clavibacter michiganensis Strains”, Microbiology, vol. 156, pp. 2366-2373, 2010.