Abstract
Potato blackleg and soft rot cause major losses and are caused by two bacterial genera, Pectobacterium and Dickeya. Species affecting potatoes are Pectobacterium atrosepticum (Pba), Pectobacterium carotovorum subsp. carotovorum (Pcc), Pectobacterium carotovorum subsp. brasiliense (Pcb), Pectobacterium wasabiae (Pwa), Dickeya dadantii (Dda) and Dickeya solani (Dso). Pathogenicity of these species is dependent on temperature, with each species having its own optimal temperature and temperature range for growth, leading to varying degrees of losses. Pectobacterium atrosepticum, a temperature sensitive species, mainly occurs in temperate climates, Pcc in temperate to tropical, and Dickeya spp. in subtropical environments. The aim of this study was to determine the cardinal growth temperatures for the species responsible for blackleg and soft rot in vitro. Bacterial isolates were incubated in a temperature gradient shaking incubator at 30 different temperatures ranging from ±5 °C to ±56 °C, and growth measured at two set time intervals. Results were statistically analysed using the Gaussian function. The optimal temperature of 31 °C and temperature range of 20 °C to 38 °C for Pectobacterium carotovorum subsp. brasiliense, was similar to those recorded for Pcc. Pectobacterium wasabiae grew at an optimal temperature of 29 °C and range of 20 °C to 34 °C. Higher optimal temperatures of 32 °C and 34 °C, with ranges of 21 °C to 38 °C and 23 °C to 41 °C were recorded for Dda and Dso, respectively. The minimal variation in optimal temperatures between different species might be an indication that temperature ranges, rather than optimal temperature, play an important role in disease development. Results for Dso, which has not yet been reported in South Africa, are especially important in light of prevailing temperatures in South African potato production regions.
Similar content being viewed by others
References
Ali, H. F., Ahmad, M., Junaid, M., Bibi, A., Ali, A., Sharif, M., Ali, B., Nawab, K., & Sadozai, A. (2012). Inoculum sources, disease incidence and severity of bacterial blackleg and soft rot of potato. Pakistan Journal of Phytopathology, 44, 825–830.
De Boer, S.H. (2004). Blackleg of potato. In: The Plant Health Instructor. http://www.apsnet.org/edcenter/intropp/lessons/prokaryotes/Pages/Blacklegpotato.aspx. Accessed 10 July 2013.
De Boer, S.H. & Kelman, A. (2001). Gram Negative Bacteria: Erwinia Soft rot Group In: N.W. Schaad, J.B. Jones & W. Chun (Eds.), Laboratory guide for the identification of plant pathogenic bacteria. 3rd Edn (pp. 56–72). St. Paul: APS Press.
Dickey, R. S. (1979). Erwinia chrysanthemi: a comparative study of phenotypic properties of strains from several hosts and other Erwinia species. Phytopathology, 69, 324–329.
Duarte, V., De Boer, S. H., Ward, L. J., & De Oliveira, A. M. R. (2004). Characterization of atypical Erwinia carotovora strains causing blackleg of potato in Brazil. Journal of Applied Microbiology, 96, 535–545.
Elphinstone, J. G. (1987). Soft rot and black leg of potato: Erwinia spp. Technical Information Bulletin, 21, 1–18.
Elphinstone, J.G. & Toth, I.K. (2007). Erwinia chrysanthemi (Dickeya spp.) The facts. In Homepage of British Potato Council Publications. www.potato.org.uk. Accessed 21 April 2008.
Gardan, L., Gouy, C., Christen, R., & Samson, R. (2003). Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. International Journal of Systematic and Evolutionary Microbiology, 53, 381–391.
Goto, M., Matsumoto, K. (1987). Erwinia carotovora subsp. wasabiae subsp. nov. isolated from diseased rhizomes and fibrous roots of Japanese Horseradish (Eutrema wasabi Maxim.). International Journal of Systematic Bacteriology, 37, 130--135.
Hauben, L., Moore, E. R., Vauterin, L., Steenackers, M., Mergaert, J., Verdonck, L. & Swings, J. (1998). Phylogenetic position of phytopathogens within the Enterobacteriaceae. Systematic Applied Microbiology, 21, 384–397.
Kushalappa, A. C., & Zulfiqar, M. (2001). Effect of wet incubation time and temperature on infection, and of storage time and temperature on soft rot lesion expansion in potatoes inoculated with Erwinia carotovora ssp. carotovora. Potato Research, 44, 233–242.
Lanham, P. G., McIlravey, K. I., & Pérombelon, M. C. M. (1991). Production of cell wall dissolving enzymes by Erwinia carotovora subsp. atroseptica in vitro at 27 °C and 30.5 °C. Journal of Applied Bacteriology, 70, 20–24.
Laurent, P., Buchon, L., Burini, J. F., & Orange, N. (2001). Low pH and cold temperature combine to limit growth and pectate lyase production by the psychrotrophic bacterium Erwinia carotovora ssp. carotovora MFCL0. Biotechnology Letters, 23, 753–756.
Laurent, P., Buchon, L., Guespin-Michel, J. F., & Orange, N. (2000). Production of pectate lyases and cellulases by Chryseomonas luteola strain MFCL0 depends on the growth temperature and the nature of the culture medium: evidence for two critical temperatures. Applied Environmental Microbiology, 66, 1538–1543.
Laurila, J., Hannukkala, A., Nykyri, J., Pasanen, M., Hélias, V., Garlant, L., & Pirhonen, M. (2010). Symptoms and yield reduction caused by Dickeya spp. strains isolated from potato and river water in Finland. European Journal of Plant Pathology, 126, 249–262.
Madigan, M.T. & Martinko, J.M. (2006). Brock Biology of Microorganisms. 11th Edn. London; Pearson Prentice Hall. 135–165.
Marquez-Villavicencio, M., Groves, R. L., & Charkowski, A. O. (2011). Soft rot disease severity is affected by potato physiology and Pectobacterium taxa. Plant Disease, 95, 232–241.
Moleleki, L. N., Onkendi, E. M., Mongae, A., & Kubheka, G. C. (2013). Characterisation of Pectobacterium wasabiae causing blackleg and soft rot diseases in South Africa. European Journal of Plant Pathology, 135, 279–288.
Molina, J. J., & Harrison, M. D. (1977). The role of Erwinia carotovora in the epidemiology of potato blackleg I. Relationship of E. carotorora var. carotovora and E. carotovora var. atroseptica to potato blackleg in Colorado. American Potato Journal, 54, 587–591.
Molina, J. J., & Harrison, M. D. (1980). The role of Erwinia carotovora in the epidemiology of potato blackleg. II. The effect of soil temperature on disease severity. American Potato Journal, 57, 351–363.
Nabhan, S., De Boer, S. H., Maiss, E., & Wydra, K. (2012). Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. Journal of Applied Microbiology, 113, 904–913.
Ngadze, E., Brady, C. L., Coutinho, T. A., & van der Waals, J. E. (2012). Pectinolytic bacteria associated with potato soft rot and blackleg in South Africa and Zimbabwe. European Journal of Plant Pathology, 134, 533–549.
Nykyri, J., Niemi, O., Koskinen, P., Nokso-Koivisto, J., Pasanen, M., Broberg, M., Plyusnin, I., Törönen, P., Holm, L., Pirhonen, M., Palva, E.T. (2012). Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathogens 8(11): e1003013. doi:10.1371/journal.ppat.1003013
Oliveira, A. M. R., Duarte, V., Silveira, J. R. P., & Moraes, M. G. (2003). Incidence of pectolytic Erwinias associated with blackleg of potato in Rio Grande do Sul. Fitopatologia Brasileira, 28, 49–53.
Pérombelon, M. C. M. (1992). Potato blackleg: epidemiology, host-pathogen interaction and control. Netherlands Journal of Plant Pathology, 98, 135–146.
Pérombelon, M. C. M. (2002). Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathology, 51, 1–12.
Pérombelon, M. C. M., & Ghanekar, A. (1979). Diseases of potato tubers – pectic enzyme production by E. carotovora. Annual Scottish Horticultural Research Institute, 1978, 31–145.
Pérombelon, M. C. M., Gullings-Handley, J., & Kelman, A. (1979). Population dynamics of Erwinia carotovorum and pectolytic Clostridia in relation to decay of potatoes. Phytopathology, 69, 167–173.
Pérombelon, M. C. M., & Hyman, L. J. (1986). A rapid method to identify and quantify soft rot Erwinias directly from plant material based on their temperature, tolerance and sensitivity to erythromycin. Journal of Applied Bacteriology, 60, 61–66.
Pérombelon, M. C. M., & Kelman, A. (1980). Ecology of the soft rot erwinias. Annual Review of Phytopathology, 18, 361–387.
Pérombelon, M. C. M., & Lowe, R. (1975). Studies on the initiation of bacterial soft rot in potato tubers. Potato Research, 18, 64–82.
Pérombelon, M. C. M., Lumb, V. M., & Zutra, D. (1987). Pathogenicity of soft rot Erwinias to potato plants in Scotland and Israel. Journal of Applied Bacteriology, 63, 73–84.
Pérombelon, M.C.M. & Salmond, G.P.C. (1995). Bacterial soft rots In: U.S Singh, R.P. Singh, K. Kohmoto, (eds) Pathogenesis and host specificity in plant diseases: Histopathological, biochemical, genetic and molecular bases, Volume 1 edn. (1–20) Great Britain: Pergamon.
Samson, R., Legendre, J. B., Christen, R., Fischer-Le Saux, M., Achouak, W., & Gardan, L. (2005). Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. International Journal of Systematic and Evolutionary Microbiology, 55, 1415–1427.
Serfontein, S., Logan, C., Swanepoel, A. E., Boelema, B. H., & Theron, D. J. (1991). A potato wilt disease in South Africa caused by Erwinia carotovora subspecies carotovora and E. chrysanthemi. Plant Pathology, 40, 382–386.
Slawiak, M., Van Beckhoven, J. R. C. M., Speksnijder, A. G. C. L., Czajkowski, R., Grabe, G., & Van der Wolf, J. M. (2009). Biochemical and genetical analysis reveal a new clade of biovar 3 Dickeya spp. strains isolated from potato in Europe. European Journal of Plant Pathology, 125, 245–261.
Smadja, B., Latour, X., Trigui, S., Burini, J. F., Chevalier, S., & Orange, N. (2004). Thermodependence of growth and enzymatic activities implicated in pathogenicity of two Erwinia carotovora subspeciess (Pectobacterium spp.). Canadian Journal of Microbiology, 50, 19–27.
Toth, I. K., Bell, K. S., Holeva, M. C., & Birch, P. R. J. (2003). Soft rot erwiniae: from genes to genomes. Molecular Plant Pathology, 4, 17–30.
Toth, I. K., Van Der Wolf, J. M., Saddler, G., Lojkowska, E., Helias, V., Pirhonen, M., Tsror, L., & Elphinstone, J. G. (2011). Dickeya species: an emerging problem for potato production in Europe. Plant Pathology, 60, 385–399.
Tsror, L., Erlich, O., Lebiush, S., Hazanovsky, M., Zig, U., Sławiak, M., Grabe, G., Van Der Wolf, J. M., & Van de Haar, J. J. (2009). Assessment of recent outbreaks of Dickeya sp. (syn. Erwinia chrysanthemi) slow wilt in potato crops in Israel. European Journal of Plant Pathology, 123, 311–320.
Tsror Lahkim, L., Ben-Daniel, B., Chalupowicz, L., Van der Wolf, J.M. Lebiush, S. Erlich, O. Dror, O. Barel, V. Nijhuis, E. Manulis-Sasson, S. (2013). Characterization of Dickeya strains isolated from potato grown under hot-climate conditions. Plant Pathology, 62, 1097–1105.
Van der Merwe, J. J. (2009). Etiology of soft rot and blackleg on potatoes in South Africa, MSc (Agric) Plant pathology. Pretoria: University of Pretoria.
Van der Merwe, J. J., Coutinho, T. A., Korsten, L., & Van der Waals, J. E. (2010). Pectobacterium carotovorum subsp. brasiliensis causing blackleg on potatoes in South Africa. European Journal of Plant Pathology, 126, 175–185.
Van der Waals, J. E., Krüger, K., Franke, A. C., Haverkort, A. J., & Steyn, J. M. (2013). Climate change and potato production in contrasting South African agro-ecosystems 3. Effects on relative development rates of selected pathogens and pests. Potato Research, 56, 67–84.
Van der Wolf, J. M., Nijhuis, E. H., Kowalewska, M. J., Saddler, G. S., Parkinson, N., Elphinstone, J. G., Pritchard, L., Toth, I. K., Lojkowska, E., Potrykus, M., Waleron, M., de Vos, P., Cleenwerck, I., Pirhonen, M., Garlant, L., Hélias, V., Pothier, J. F., Pflüger, V., Duffy, B., Tsror, L., & Manulis, S. (2014). Dickeya solani sp. nov., a pectinolytic plant-pathogenic bacterium isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology, 64, 768–774.
Waleron, M., Waleron, K., & Lojkowska, E. (2013). Occurrence of Pectobacterium wasabiae in potato field samples. European Journal of Plant Pathology, 137, 149–158.
Acknowledgments
The authors would like to thank Marie Smith for help with the statistical analyses, and The Technology and Human Resources in Industry Programme (THRIP) and Potatoes South Africa for funding this work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
du Raan, S., Coutinho, T.A. & van der Waals, J.E. Cardinal temperature differences, determined in vitro, between closely related species and subspecies of pectinolytic bacteria responsible for blackleg and soft rot on potatoes. Eur J Plant Pathol 144, 361–369 (2016). https://doi.org/10.1007/s10658-015-0773-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-015-0773-x