Harnessing the bacteriophages to deal with canker infection of kiwi fruit: challenges and future perspective

Ali  Raza; Musharaf  Hassan; Sara  Janiad; Aamir  Riaz; Ali  Khan; Zia Ur  Rehman; Muhammad  Saleem

Authors

Ali Raza University of OKara https://orcid.org/0000-0002-1165-0995
Musharaf Hassan Department of Computer Science, University of Agriculture Faisalabad, Pakistan https://orcid.org/0009-0007-9236-5718
Sara Janiad Department of Microbiology & Molecular Genetics, Women University of Multan, Punjab, Pakistan https://orcid.org/0000-0002-3969-8114
Aamir Riaz Department of Microbiology & Molecular Genetics, University of Okara, Punjab, Pakistan https://orcid.org/0000-0003-1693-277X
Ali Khan Department of Microbiology & Molecular Genetics, University of Okara, Punjab, Pakistan https://orcid.org/0009-0002-5490-9263
Zia Ur Rehman Department of Microbiology & Molecular Genetics, University of Okara, Punjab, Pakistan
Muhammad Saleem Department of Molecular Biology, University of Okara, Punjab, Pakistan

Keywords:

Bacteriophages, Pseudomonas syringae pv. actinidiae (Psa), lytic activity, phage therapy, environmental adaptation

Abstract

The worldwide kiwifruit industry has suffered significant economic losses in recent decades as a result of the destructive bacterial plant disease Pseudomonas syringae pv. actinidiae (Psa). Existing control approaches, which depend on the use of copper bactericides and antibiotics, are facing growing challenges due to the rise of resistance to antibiotics and ecological issues. Although biocontrol techniques show promise in laboratory settings, their efficacy in real-world field situations remains unclear. In order to tackle this issue, the emergence of a phage-based biocontrol method becomes a vital alternative, considering the precise targeting of bacteriophages (phages) towards the particular bacteria and their ecologically benign characteristics. This thorough assessment commences by delineating the repercussions of Psa-induced kiwifruit canker, underscoring the need for pioneering management strategies. The text explores the many types and strengths of Psa strains, and then shifts its attention to recent progress in the identification and description of Psa phages. The main topics discussed are the physical structure of phages, the spectrum of organisms they may infect, their ability to destroy bacterial cells, the study of their genetic material, and the process by which they break down bacterial cells. The review examines biocontrol tactics and their possible obstacles in kiwifruit orchards, specifically focusing on abiotic variables such as elevated temperature, UV irradiation and severe pH. The manuscript highlights the crucial importance of phages in efficiently controlling Psa infections, providing a sustainable and focused approach for safeguarding plants.

References

Buttimer, C., McAuliffe, O., Ross, R. P., Hill, C., O’Mahony, J., & Coffey, A. (2017). Bacteriophages and bacterial plant diseases. Frontiers in Microbiology, 8, 34.

Camiring, A. D. (2022). Genetic Analysis of Daylength-dependent Bulb Formation Genes and Development of Protocol for Agrobacterium-Mediated Transformation of Onion (Allium cepa L.). University of Otago,

Chegini, Z., Khoshbayan, A., Taati Moghadam, M., Farahani, I., Jazireian, P., & Shariati, A. (2020). Bacteriophage therapy against Pseudomonas aeruginosa biofilms: A review. Annals of clinical microbiology and antimicrobials, 19, 1-17.

Chen, Y., Feng, X., Ren, H., Yang, H., Liu, Y., Gao, Z., & Long, F. (2020). Changes in physicochemical properties and volatiles of kiwifruit pulp beverage treated with high hydrostatic pressure. Foods, 9(4), 485.

Córdova, P., Rivera-González, J. P., Rojas-Martínez, V., Fiore, N., Bastías, R., Zamorano, A., . . . Ilabaca-Díaz, C. (2023). Phytopathogenic Pseudomonas syringae as a Threat to Agriculture: Perspectives of a Promising Biological Control Using Bacteriophages and Microorganisms. Horticulturae, 9(6), 712.

Di Lallo, G., Evangelisti, M., Mancuso, F., Ferrante, P., Marcelletti, S., Tinari, A., . . . Frezza, D. (2014). Isolation and partial characterization of bacteriophages infecting Pseudomonas syringae pv. actinidiae, causal agent of kiwifruit bacterial canker. Journal of Basic Microbiology, 54(11), 1210-1221.

Donati, I., Cellini, A., Sangiorgio, D., Vanneste, J. L., Scortichini, M., Balestra, G. M., & Spinelli, F. (2020). Pseudomonas syringae pv. actinidiae: Ecology, infection dynamics and disease epidemiology. Microbial ecology, 80, 81-102.

Dwiartama, A. (2017). Resilience and transformation of the New Zealand kiwifruit industry in the face of Psa-V disease. Journal of rural studies, 52, 118-126.

Flores, O., Retamales, J., Núñez, M., León, M., Salinas, P., Besoain, X., . . . Bastías, R. (2020). Characterization of bacteriophages against Pseudomonas syringae pv. actinidiae with potential use as natural antimicrobials in kiwifruit plants. Microorganisms, 8(7), 974.

Frampton, R. A., Lopez Acedo, E., Young, V. L., Chen, D., Tong, B., Taylor, C., . . . Bostina, M. (2015). Genome, proteome and structure of a T7-like bacteriophage of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Viruses, 7(7), 3361-3379.

Frampton, R. A., Taylor, C., Holguín Moreno, A. V., Visnovsky, S. B., Petty, N. K., Pitman, A. R., & Fineran, P. C. (2014). Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Applied and Environmental Microbiology, 80(7), 2216-2228.

Grace, E. R., Rabiey, M., Friman, V. P., & Jackson, R. W. (2021). Seeing the forest for the trees: Use of phages to treat bacterial tree diseases. Plant Pathology, 70(9), 1987-2004.

Hagens, S., & Loessner, M. J. (2010). Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Current pharmaceutical biotechnology, 11(1), 58-68.

Huang, S., Ding, J., Deng, D., Tang, W., Sun, H., Liu, D., . . . Meng, M. (2013). Draft genome of the kiwifruit Actinidia chinensis. Nature communications, 4(1), 2640.

Kannoly, S., Oken, G., Shadan, J., Musheyev, D., Singh, K., Singh, A., & Dennehy, J. J. (2023). Single-cell approach reveals intercellular heterogeneity in phage-producing capacities. Microbiology Spectrum, 11(1), e02663-02621.

Kazi, M., & Annapure, U. S. (2016). Bacteriophage biocontrol of foodborne pathogens. Journal of food science and technology, 53, 1355-1362.

Kilcher, S., Studer, P., Muessner, C., Klumpp, J., & Loessner, M. J. (2018). Cross-genus rebooting of custom-made, synthetic bacteriophage genomes in L-form bacteria. Proceedings of the National Academy of Sciences, 115(3), 567-572.

Kim, K.-H., & Koh, Y. J. (2019). An integrated modeling approach for predicting potential epidemics of bacterial blossom blight in kiwifruit under climate change. The plant pathology journal, 35(5), 459.

Kranjec, C., Morales Angeles, D., Torrissen Mårli, M., Fernández, L., García, P., Kjos, M., & Diep, D. B. (2021). Staphylococcal biofilms: Challenges and novel therapeutic perspectives. Antibiotics, 10(2), 131.

Lai, W. C. B., Chen, X., Ho, M. K. Y., Xia, J., & Leung, S. S. Y. (2020). Bacteriophage-derived endolysins to target gram-negative bacteria. International Journal of Pharmaceutics, 589, 119833.

Lee, Y. S., Kim, G. H., Koh, Y. J., & Jung, J. S. (2020). Evaluation of the Genetic Diversity of Biovar 3 Strains of Pseudomonas syringae pv. actinidiae Isolated in Korea. 생명과학회지, 30(1), 1-9.

Liao, Y.-T., Salvador, A., Harden, L. A., Liu, F., Lavenburg, V. M., Li, R. W., & Wu, V. C. (2019). Characterization of a lytic bacteriophage as an antimicrobial agent for biocontrol of shiga toxin-producing Escherichia coli O145 strains. Antibiotics, 8(2), 74.

Liu, Y., Liu, M., Hu, R., Bai, J., He, X., & Jin, Y. (2021). Isolation of the novel phage PHB09 and its potential use against the plant pathogen Pseudomonas syringae pv. actinidiae. Viruses, 13(11), 2275.

Luo, J., Dai, D., Lv, L., Ahmed, T., Chen, L., Wang, Y., . . . Li, B. (2022). Advancements in the Use of Bacteriophages to Combat the Kiwifruit Canker Phytopathogen Pseudomonas syringae pv. actinidiae. Viruses, 14(12), 2704.

Mandal, M., Das, S., Roy, A., Rakwal, R., Jones, O. A., Popek, R., . . . Sarkar, A. (2023). Interactive relations between plants, phyllosphere microbial community, and particulate matter pollution. Science of The Total Environment, 164352.

Martino, G., Holtappels, D., Vallino, M., Chiapello, M., Turina, M., Lavigne, R., . . . Ciuffo, M. (2021). Molecular Characterization and Taxonomic Assignment of Three Phage Isolates from a Collection Infecting Pseudomonas syringae pv. actinidiae and P. syringae pv. phaseolicola from Northern Italy. Viruses, 13(10), 2083.

Mazzaglia, A., Studholme, D. J., Taratufolo, M. C., Cai, R., Almeida, N. F., Goodman, T., . . . Balestra, G. M. (2012). Pseudomonas syringae pv. actinidiae (PSA) isolates from recent bacterial canker of kiwifruit outbreaks belong to the same genetic lineage. PLoS One, 7(5), e36518.

Ni, P., Wang, L., Deng, B., Jiu, S., Ma, C., Zhang, C., . . . Wang, S. (2020). Combined application of bacteriophages and carvacrol in the control of Pseudomonas syringae pv. actinidiae planktonic and biofilm forms. Microorganisms, 8(6), 837.

Ni, P., Wang, L., Deng, B., Jiu, S., Ma, C., Zhang, C., . . . Wang, S. (2021). Characterization of a lytic bacteriophage against Pseudomonas syringae pv. actinidiae and its endolysin. Viruses, 13(4), 631.

Panno, S., Davino, S., Caruso, A. G., Bertacca, S., Crnogorac, A., Mandić, A., . . . Matić, S. (2021). A review of the most common and economically important diseases that undermine the cultivation of tomato crop in the mediterranean basin. Agronomy, 11(11), 2188.

Patra, S. K., & Roy, U. (2023). Is Open Science a Developed Countries’ Phenomenon? A Case Study of Journals Registered in the DOAJ. Qeios.

Piergentili, R., Del Rio, A., Signore, F., Umani Ronchi, F., Marinelli, E., & Zaami, S. (2021). CRISPR-Cas and its wide-ranging applications: From human genome editing to environmental implications, technical limitations, hazards and bioethical issues. Cells, 10(5), 969.

Pinheiro, L. A., Pereira, C., Barreal, M. E., Gallego, P. P., Balcão, V. M., & Almeida, A. (2020). Use of phage ϕ6 to inactivate Pseudomonas syringae pv. actinidiae in kiwifruit plants: In vitro and ex vivo experiments. Applied microbiology and biotechnology, 104, 1319-1330.

Pinheiro, L. A., Pereira, C., Frazão, C., Balcão, V. M., & Almeida, A. (2019). Efficiency of phage φ6 for biocontrol of Pseudomonas syringae pv. syringae: an in vitro preliminary study. Microorganisms, 7(9), 286.

Savian, F. (2020). New strategies to study and control plant diseases and their application to Kiwifruit Decline.

Sharma, K., Kumar, R., & Kumar, A. (2022). Himalayan Horticulture Produce Supply Chain Disruptions and Sustainable Business Solution—A Case Study on Kiwi Fruit in Uttarakhand. Horticulturae, 8(11), 1018.

Song, Y.-R., Vu, N. T., Park, J., Hwang, I. S., Jeong, H.-J., Cho, Y.-S., & Oh, C.-S. (2021). Phage PPPL-1, a new biological agent to control bacterial canker caused by Pseudomonas syringae pv. actinidiae in Kiwifruit. Antibiotics, 10(5), 554.

Tahir, J., Hoyte, S., Bassett, H., Brendolise, C., Chatterjee, A., Templeton, K., . . . Morgan, E. (2019). Multiple quantitative trait loci contribute to resistance to bacterial canker incited by Pseudomonas syringae pv. actinidiae in kiwifruit (Actinidia chinensis). Horticulture Research, 6.

Wójcicki, M., Błażejak, S., Gientka, I., & Brzezicka, K. (2019). The concept of using bacteriophages to improve the microbiological quality of minimally processed foods. Acta Scientiarum Polonorum Technologia Alimentaria, 18(4), 373-383.

Yang, Y., Ma, R., Yu, C., Ye, J., Chen, X., Wang, L., . . . Zhang, R. (2022). A novel alteromonas phage lineage with a broad host range and small burst size. Microbiology Spectrum, 10(4), e01499-01422.

Yin, Y., Ni, P. e., Deng, B., Wang, S., Xu, W., & Wang, D. (2019). Isolation and characterisation of phages against Pseudomonas syringae pv. actinidiae. Acta Agriculturae Scandinavica, Section B—Soil & Plant Science, 69(3), 199-208.

Yu, J.-G., Lim, J.-A., Song, Y.-R., Heu, S., Kim, G. H., Koh, Y. J., & Oh, C.-S. (2016). Isolation and characterization of bacteriophages against Pseudomonas syringae pv. actinidiae causing bacterial canker disease in kiwifruit. Journal of microbiology and biotechnology, 26(2), 385-393.

Żbikowska, K., Michalczuk, M., & Dolka, B. (2020). The use of bacteriophages in the poultry industry. Animals, 10(5), 872.

Zeaki, N., Johler, S., Skandamis, P. N., & Schelin, J. (2019). The role of regulatory mechanisms and environmental parameters in staphylococcal food poisoning and resulting challenges to risk assessment. Frontiers in Microbiology, 10, 1307.

Zhang, R., Weinbauer, M. G., & Peduzzi, P. (2021). Aquatic viruses and climate change. Current Issues in Molecular Biology, 41(1), 357-380.