Potentially dangerous causes of bacterial diseases of potatoes in Ukraine

Yuliia Kolomyets, L. Butsenko
Abstract

An overview of bacterial causative agents of soft (wet) rot of potatoes is given, the epidemiological and etiological aspects of the diseases caused by them are analyzed. When preparing the article, general scientific methods were used: generalization, comparison, system analysis. Data from the European and Mediterranean Plant Protection Organization (EOPO), as well as data from phytosanitary services of EU countries and Ukraine, scientific literature served as material for the analytical study. Trade in plant materials, including potato seed tubers and ornamental plants, is largely responsible for the widespread distribution of pathogens. Locally, pathogens are also spread through plant debris, soil, waterways, aerosols, alternative hosts, and/or farm machinery. The main causative agents of bacterial wet rot of potatoes are gramnegative bacteria of the genera Pectobacterium and Dickeya and quarantine phytopathogens of the genera Clavibacter and Ralstonia. The main methods of detection and identification in asymptomatic potato tubers on an industrial scale are: phytopathological (visual examination of plantations and registration of symptoms of soft rot), microbiological (cultural-morphological and biochemical method, use of test systems for accelerated identification of microorganisms), immunoenzymatic ( enzyme immunosorbent assay), molecular genetic (PCR with specific primers, BIOLOG, DNA fingerprinting and nucleotide sequencing). To date, there are no completely effective pesticides to control all pathogens, so disease control measures will continue to rely primarily on avoiding infection during plant cultivation, and especially during the production of healthy certified seed. For a crop like potatoes, this is primarily based on obtaining bacteria-free minibulbs, applying strict seed certification schemes and strict phytosanitary restrictions. Knowledge of the sources of pathogens and routes of infection should be the basis for the application of phytosanitary measures, especially during and after harvest. Control of quarantine phytopathogens requires special attention. Soft rot pathogens are the main cause of limiting potato production in many regions of the world, particularly Clavibacter michiganensis subsp. sepedonicum and R. solanacearum are quarantine objects of the A-2 list of the European and Mediterranean Organization for Quarantine and Plant Protection. Upon entering our country, R. solanacearum has a high probability of acclimatization and spread in the country

Keywords

Solanum tuberosum L.; wet (soft) rot; phytopathogenic bacteria; pathogen control; plant quarantine

Suggested citation
Kolomyets, Yu., & Butsenko, L. (2023). Potentially dangerous causes of bacterial diseases of potatoes in Ukraine. Biological Systems: Theory and Innovation, 14(1), 26-44. https://doi.org/10.31548/biologiya14(1-2).2023.002
References

[1] Aslam, M.N., Mukhtar, T., Hussain, M.A., & Raheel, M. (2017). Assessment of resistance to bacterial wilt incited by Ralstonia solanacearum in tomato germplasm. Journal of Plant Disease Protection, 124, 585-590. doi: 10.1007/s41348-017-0100-1

[2] Baştaş, K.K., Hekimhan, H., Maden, S., & Tör, M. (2009). First report of bacterial stalk and head rot disease caused by Pectobacterium atrosepticum on sunflower in Turkey. Plant Disease,   93(12), article number 1352. doi: 10.1094/PDIS-93-12-1352B.

[3] Birch, P.R., Bryan, G., Fenton, B., Gilroy, E.M., Hein, I., Jones, J.T., & Toth, I.K. (2012). Crops that feed the world 8: Potato: Are the trends of increased global production sustainable? Food Security, 4(4), 477-508, doi: 10.1007/s12571-012-0220-1.   

[4] Birhane, E., Hailemariam, M., Gebresamuel, G., et al. (2020). Source of mycorrhizal inoculum influences growth of Faidherbia albida seedlings. Journal of Forestry Research, 31(1), 313-323. doi: 10.1007/s11676-018-0810-7.  

[5] Bragard, C., Dehnen-Schmutz, K., Serio, F., di Gonthier, P., Miret, J.A.J., Justesen, A.F., MacLeod, A., Magnusson, C.S., Milonas, P., Navas-Cortes, J.A., Parnell, S., Potting, R., Reignault, P.L., Thulke, H.H., Werf, W., van der Civera, A.V., Yuen, J., Zappalà, L., Wolf, J., van der Kaluski, T., Pautasso, M., & Jacques, M.A. (2019). Pest categorisation of Clavibacter sepedonicusEuropean Food Safety Authority Journal, 17(4), p. 05670. doi: 10.2903/j.efsa.2019.5670.  

[6] CABI (2006). Clavibacter michiganensis subsp. sepedonicusdoi: 10.1079/DMPD/20066500020.

[7] Charkowski, A., Blanco, C., Condemine, G., Expert, D., Franza, T., Hayes, C., Hugouvieux-Cotte-Pattat, N., López, Solanilla, E., Low, D., Moleleki, L., Pirhonen, M., Pitman, A., Perna, N., Reverchon, S., Rodríguez-Palenzuela, P., San, Francisco, M., Toth, I., Tsuyumu, S., van der Waals, J., van der Wolf, J., van Gijsegem, F., Yang, C.H., Yedidia, I. (2012). The role of secretion systems and small molecules in soft-rot enterobacteriaceae pathogenicity. Annual Reviews Phytopathology, 50, 425-449. doi: 10.1146/annurev-phyto-081211-173013.  

[8] Charkowski, A., Sharma, K., Parker, M.L., Secor, G.A., & Elphinstone, J. (2020). Bacterial Diseases of Potato. In H. Campos, & O. Ortiz. (Eds.). The Potato Crop (pp. 351-388). Switzerland: Springer Nature Switzerland. doi: 10.1007/978-3-030-28683-5_10.  

[9] Charkowski, A.O. (2015). Biology and control of Pectobacterium in potato. American Journal of Potato Research, 92(2), 223-229. doi: 10.1007/s12230-015-9447-7.

[10] Charkowski, A.O. (2018). The changing face of bacterial soft-rot diseases. Annual Review of Phytopathology, 56(1), 269-288. doi: 10.1146/annurev-phyto-080417-045906.  

[11] Commission Directive No. 2006/63/EC “On Amending Annexes II to VII to Council Directive 98/57/EC On the Control of Ralstonia Solanacearum (Smith) Yabuuchi et al”.(2006, July). Retrieved from https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32006L0063.  

[12] Cray, J.A., Connor, M.C., Stevenson, A., Houghton, J.D.R., Rangel, D.E.N., Cooke, L.R., & Hallsworth, J.E. (2016). Biocontrol agents promote growth of potato pathogens, depending on environmental conditions. Microbial Biotechnology, 9(3), 330-354. doi: 10.1111/1751-7915.12349.

[13] Curland, R.D., Mainello, A., Perry, K.L., Hao, J., Charkowski, A.O., Bull, C.T., et al. (2021). Species of Dickeya and Pectobacterium isolated during an outbreak of blackleg and soft rot of potato in northeastern and north Central United States. Microorganisms, 9(8), article number 1733. doi: 10.3390/microorganisms9081733.  

[14] Czajkowski, R., de Boer, W.J., Velvis, H.,   & van der Wolf, J. (2010). Systemic colonization of potato plants by a soilborne, green fluorescent protein-tagged strain of Dickeya sp. biovar 3. Phytopathology, 100(2), 134-142. doi: 10.1094/PHYTO-100-2-0134.

[15] De Boer, S.H., Elphinstone, J.G., & Schaad, N.W. (2017). Detection of Clavibacter michiganensis subsp. Sepedonicus in potato tubers. In M. Fatmi, R.R. Walcott & N.W. Schaad. (Eds.). Detection of plant-pathogenic bacteria in seed and other planting material, 2nd edition (pp. 205-209). Minnesota: American Phytopathological Society.

[16] Dees, M.W., Lebecka, R., Perminow, J.I.S., et al. (2017). Characterization of Dickeya and Pectobacterium strains obtained from diseased potato plants in different climatic conditions of Norway and Poland. European Journal of Plant Pathology, 148, 839-851. doi: 10.1007/s10658-016-1140-2.

[17] Elmer, W.H., & Datnoff, L.E. (2014). Mineral nutrition and suppression of plant disease.   New York: Academic Press. doi: 10.1016/B978-0-444-52512-3.00251-5.  

[18] EPPO (n.d.). Global database. Retrieved https://gd.eppo.int/.

[19] European Food Safety Authority, Schenk M, Camilleri M, Diakaki M and Vos S (2019). Pest survey card on Clavibacter michiganensis subsp. sepedonicusEuropean Food Safety Authority Supporting Publication, 16(2), 1-18. doi: 10.2903/sp.efsa.2019.EN-1569.

[20] Fikowicz-Krosko, J., & Czajkowski, R. (2018). Systemic colonization and expression of disease symptoms on bittersweet nightshade (Solanum dulcamara) infected with a GFP-tagged Dickeya solani IPO2222 (IPO2254). Plant Disease, 102(3), 619-627. doi: 10.1094/PDIS-08-17-1147-RE.  

[21] García, R.O., Kerns, J.P., & Thiessen, L. (2019). Ralstonia solanacearum species complex: A quick diagnostic guide. Plant Health Progress, 20(1), 7-13. doi: 10.1094/PHP-04-18-0015-DG.

[22] Golanowska, M., Kielar, J., & Lojkowska, E. (2017). The effect of temperature on the phenotypic features and the maceration ability of Dickeya solani strains isolated in Finland, Israel and Poland. European Journal of Plant Pathology, 147(4), 803-817. doi: 10.1007/s10658-016-1044-1.

[23] Golanowska, M., Potrykus, M., Motyka-Pomagruk, A., Kabza, M., Bacci, G., Galardini, M., Bazzicalupo, M., Makalowska, I., Smalla, K., Mengoni, A., Hugouvieux-Cotte-Pattat, N., & Lojkowska, E. (2018). Comparison of highly and weakly virulent Dickeya solani strains, with a view on the pangenome and panregulon of this species. Frontiers in Microbiology, 9, article   number 1940. doi: 10.3389/fmicb.2018.01940.

[24] Gryń, G., Franke, K., Nowakowski, M.M., & Nowakowski, M. (2020). Latent infection by Clavibacter sepedonicus and correlation with ring rot symptoms development in potato cultivars. Potato Research, 64, 459-468. doi: 10.1007/s11540-020-09486-6.  

[25] Hadizadeh, I., Peivastegan, B., Hannukkala, A., van der Wolf, J., Nissinen, R., & Pirhonen, M. (2019). Biological control of potato soft rot caused by Dickeya solani and the survival of bacterial antagonists under cold storage conditions. Plant Pathology, 68, 297-311. doi: 10.1111/ppa.12956.  

[26] Hashemi-Tameh, M., Primiceri, E., Chiriacò, M.S., Poltronieri, P., Bahar, M., Maruccio, G.J.B. (2020). Pectobacterium atrosepticum biosensor for monitoring blackleg and soft rot disease of potato. Biosensors (Basel), 10(6), article number 64. doi: 10.3390/bios10060064.

[27] Huber, D., Römheld, V., & Weinmann, M. (2012). Relationship between nutrition, plant diseases and pests. In Marschner’s mineral nutrition of higher plants (third edition) (pp. 283-298). Cambridge: Academic Press. doi: 10.1016/B978-0-12-384905-2.00010-8.  

[28] Huber, D.M., & Thompson, I.A. (2007). Nitrogen and plant disease. In: L.E. Datnoff, W.H. Elmer, & D.M. Huber (Eds.), Mineral nutrition and plant disease (pp. 31-44). Minnesota: American Phytopathological Society.  

[29] Karim, Z., & Hossain, M.S. (2018). Management of bacterial wilt (Ralstonia solanacearum) of potato: Focus on natural bioactive compounds. Journal of Biodiversity Conservation and Bioresource Management, 4(1), 73-92.
doi: 10.3329/jbcbm.v4i1.37879.  

[30] Khairy, A.M., Tohamy, M.R.A, Zayed, M.A., Ali, M.A.S. (2021). Detecting pathogenic bacterial wilt disease of potato using biochemical markers and evaluate resistant in some cultivars. Saudi Journal of Biological Sciences, 28(9), 5193-5203. doi: 10.1016/j.sjbs.2021.05.045.

[31] Li, X., Tambong, J., Yuan, K.X., Chen, W., Xu, H., Lévesque, C.A., & Boer, S.H.De. (2018). Re-classification of Clavibacter michiganensis subspecies on the basis of whole-genome and multi-locus sequence analyses. International Journal of   Systematic Evolutionary Microbiology, 68(1), 234-240.   doi.org: 10.1099/ijsem.0.002492.

[32] Mackay, I.M. (2004). Real-time PCR in the microbiology laboratory. Clinical Microbiology and Infection, 10(3): 190-212. doi: 10.1111/j.1198-743X.2004.00722.x.

[34] Marquez-Villavicencio, M.D.P., Groves, R.L., & Charkowski, A.O. (2011). Soft rot disease severity is affected by potato physiology and Pectobacterium taxa. Plant Disease, 95, 232-241. doi: 10.1094/PDIS-07-10-0526.

[35] Milling, A., Babujee, L., & Allen, C. (2011). Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS One, 6(1), e15853. doi: 10.1371/journal.pone.0015853.

[36] Mills, A., & Hurta, R. (2006). Sensitivity of Erwinia spp. to salt compounds in vitro and their effect on the development of soft rot in potato tubers in storage. Postharvest Biology and Technology, 41(2), 208-214. doi: 10.1016/j.postharvbio.2006.03.015.

[37] Motyka-Pomagruk, A., Zoledowska, S., Sledz, W. et al. (2021). The occurrence of bacteria from different species of Pectobacteriaceae on seed potato plantations in Poland. European Journal of Plant Pathology, 159, 309-325. doi: 10.1007/s10658-020-02163-x.  

[38] Mumford, R., Boonham, N., Tomlinson, J., & Barker, I. (2006). Advances in molecular phytodiagnostics – new solutions for old problems. European Journal of Plant Pathology, 116(1), 1-19. doi: 10.1007/s10658-006-9037-0.  

[39] Mutimawurugo, M.C., Wagara, I.N., Muhinyuza, J.B., & Ogweno, J.O. (2019). Virulence and characterization of isolates of potato bacterial wilt caused by Ralstonia solanacearum (Smith) in Rwanda. African Journal of Agricultural Research, 14(6), 311-320, article number 09A091660182. Retrieved from https://academicjournals.org/journal/AJAR/article-references/09A091660182.

[40] Osdaghi, E, van der Wolf, J.M., Abachi, H., Li, X., de Boer, S.H., & Ishimaru, C.A. (2022). Bacterial ring rot of potato caused by Clavibacter sepedonicus: A successful example of defeating the enemy under international regulations. Molecular Plant Pathology, 23(7), 911-932. doi: 10.1111/mpp.13191.

[41] Oztruk, M., Aksoy, H.M., Potrykus, M., & Lojkowska, E. (2018) Genotypic and phenotypic variability of Pectobacterium strains causing blackleg and soft rot on potato in Turkey. European Journal of Plant Pathology, 152, 143-155. doi: 10.1007/s10658-018-1459-y.

[42] Pastrik, K.H., Elphinstone, J., Pukall, R. (2002). Sequence analysis and detection of Ralstonia solanacearum by Multiplex PCR Amplification of 16S-23S ribosomal intergenic spacer region with internal positive control. European Journal of Plant Pathology, 108, 831-842. doi: 10.1023/A:1021218201771.  

[43] Polozhenets, V., & Nemerytska,   L. (2019). Diagnosis, symptoms and sources of infection of the black stalk of the potato. Scientific reports of the National University of Life and Environmental Sciences of Ukraine, 6(82), 1-6. doi: 10.31548/dopovidi2019.06.002.

[44] Potrykus, M., Golanowska, M., Sledz, W., Zoledowska, S., Motyka, A., Kolodziejska, A., Butrymowicz, J., & Lojkowska, E. (2016). Biodiversity of Dickeya spp. isolated from potato plants and water sources in temperate climate. Plant Disease, 100(2), 408-417. doi: 10.1094/PDIS-04-15-0439-RE.

[45] Puaprasert, K., Chu, C., Saralamba, N., Day, N.P., Nosten, F., White, N.J., & Imwong, M. (2018). Real time PCR detection of common CYP2D6 genetic variants and its application in a Karen population study. Malaria Journal, 17(1), 427, https://doi.org/10.1186/s12936-018-2579-8.

[46] Review of the spread of quarantine organisms in Ukraine. (n.d.). Retrieved from https://dpss.gov.ua/fitosanitariya-kontrol-u-sferi-nasinnictva-ta-rozsadnictva/fitosanitarnij-kontrol/oglyad-poshirennya-karantinnih-organizmiv-v-ukrayini.

[47] Robert, M. (2013). General aspects of the prevention and control of the potato ring rot disease (Clavibacter michiganensis subsp. sepedonicus). Journal of Horticulture, Forestry and Biotechnology, 17, 122-124. Retrieved from https://www.cabidigitallibrary.org/doi/pdf/10.5555/20133364731.

[48] Rossmann, S., Dees, M.W., Perminow, J., Meadow, R., & Brurberg, M.B. (2018). Soft rot Enterobacteriaceae are carried by a large range of insect species in potato fields. Applied and Environmental Microbiology, 84(12), 00281-00218. doi: 10.1128/AEM.00281-18.  

[49] Sagar, V., Jeevalatha, A., Mian, S., Chakrabarti, S.K., Gurjar, M.S., Arora, R.K., & Singh, B.P. (2014). Potato bacterial wilt in India caused by strains of phylotype I, II and IV of Ralstonia solanacearumEuropean Journal of Plant Pathology, 138(1), 51-65. doi: 10.1007/s10658-013-0299-z.  

[50] Stridh, L.J., Mostafanezhad, H., Andersen, C.B., et al. (2022). Reduced efficacy of biocontrol agents and plant resistance inducers against potato early blight from greenhouse to field. Journal of Plant Diseases and Protection, 129, 923-938. doi: 10.1007/s41348-022-00633-4.  

[51] Timko, L.V. (2017). Evaluation of the parameters of the adaptive capacity of potato varieties in the conditions of the Right Bank Polissia of Ukraine. Potato production of Ukraine, 1-2(42–43),   18-22.***

[52] Toth, I.K., Hyman, L.J., & Wood, J.R. (1999). A one step PCR-based method for the detection of economically important soft rot Erwinia species on micropropagated potato plants. Journal of Applied Microbiology, 87(1), 158-166. doi: 10.1046/j.1365-2672.1999.00808.x.    

[53] Toth, I.K., van der Wolf, J.M., Saddler, G., Lojkowska, E., Hélias, V., Pirhonen, M., Tsror (Lahkim), L., Elphinstone, J.G. (2011). Dickeya species: An emerging problem for potato production in Europe. Plant Pathology, 60(3), 385-399. doi: 1111/j.1365-3059.2011.02427.x.  

[54] Uwamahoro, F., Berlin, A., Bucagu, C., Bylund, H., & Yuen, J. (2020). Ralstonia solanacearum causing potato bacterial wilt: Host range and cultivars susceptibility in Rwanda. Plant Pathology, 69(3), 559-568. doi: 10.1111/ppa.13140.

[55] van der Wolf, J.M., de Boer, S.H., Czajkowski, R., Cahill, G., van Gijsegem, F., Davey, T., Brice-Dupuis, B., Ellicott, J., Jafra, S., Kooman, M., Toth, I.K., Tsror, L., Yedidia, I., & van der Waals, J.E. (2021). Management of diseases caused by Pectobacterium and Dickeya species. In Plant diseases caused by Dickeya and Pectobacterium species (pp. 175-214). Switzerland: Springer. doi: 10.1007/978-3-030-61459-1_6.

[56] van der Wolf, J.M., Elphinstone, J.G., Stead, D.E., Metzler, M., Müller, P., Hukkanen, A., & Karjalainen, R. (2005). Epidemiology of Clavibacter michiganensis subsp. sepedonicus in relation to control of bacterial ring rot. Retrieved from https://edepot.wur.nl/39352.  

[57] van der Wolf, J.M., Nijhuis, E.H., & Kowalewska, M.J. (2014). Dickeya solani sp. nov., a pectinolytic plant pathogenic bacterium isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology, 64(3), 768-774. doi: 10.1099/ijs.0.052944-0.

[58] Wei, Y., Moreno, C.C., Gongora, T.J., Wang, K., Sang, Y., Duran, R.L., & Macho, A.P. (2018). The Ralstonia solanacearum csp22 peptide, but not flagellin-derived peptides, is perceived by plants from the solanaceae family. Journal of Plant Biotechnology, 16(7), 1349-1362. doi: 10.1111/pbi.12874.

[59] White, P.J., & Broadley, M.R. (2003). Calcium in plants. Annals of Botany, 92(4), 487-511. doi: 10.1093/aob/mcg164.