Raoultella terrigena and Pectobacterium carotovorum in vegetables in two provinces of Costa Rica
DOI:
https://doi.org/10.15517/am.v32i1.40845Keywords:
soft rot, phytopathology, molecular analysisAbstract
Introduction. Soft rot in crops is caused by a group of bacteria capable of secreting enzymes that degrade pectin in the cell wall of the plants and causes significant economic losses in agriculture worldwide. In Costa Rica, there is few data available about the distribution, hosts, and genetic diversity of the causal agents of disease. Objective. To identify the presence of bacteria causing soft rot in vegetables located in Cartago and Alajuela using molecular and enzymatic analysis, and pathogenicity techniques. Materials and methods. The study was carried out between July and October 2017 in Cartago and Alajuela, Costa Rica. Plants with soft roth symptoms were collected: sweet chili (Capcicum annum), onion leaves and bulbs (Allium cepa), zucchini plants (Cucurbita pepo), tomato fruits (Solanum lycopersicum), and potato plants (Solanum tuberosum). Bacterial isolation was performed on a selective violet crystal and pectate (CVP) medium. Hypersensitive reaction (RH) tests were performed, the isolates were inoculated into sweet chili leaves and pathogenicity tests (Koch´s postulates) were carried out for the positive bacteria. The isolates were identified by the 16S RNA-Ribosomal gene. Results. Five bacteria with pectinolytic activity were isolated: Pt1-A, 6-M2, Ech2A, CfspA, and Cfsab. According to the pathogenicity analysis, CfspA, Cfsab, and Ech2A strains were causal agents of soft rot in chile. It was not possible to reproduce the symptoms in onion and potato. According to the molecular identification, CfspA and Cfsab strains were classified within the Pectobacterium carotovorum clade, while Ech2A was classified as Raoultella terrigena. Conclusion. Raoultella and Pectobacterium carotovorum were considered the causal agents of soft rotting of chili in the areas of Cartago and Alajuela respectively.
Downloads
References
Agrios, G. N. (2005). Plant Pathology (5th ed.). Elsevier.
Arauz, L. (2011). Fitopatología: Un enfoque agroecológico (5ª ed.). Editorial Universidad de Costa Rica.
Asai, S., & Shirasu, K. (2015). Plant cells under siege: Plant immune system versus pathogen effectors. Current Opinion in Plant Biology, 28, 1–8. https://doi.org/10.1016/j.pbi.2015.08.008
Barny, M. A. (1995). Erwinia amylovora hrpN mutants, blocked in harpin synthesis, express a reduced virulence on host plants and elicit variable hypersensitive reactions on tobacco. European Journal of Plant Pathology, 101(3), 333–340. https://doi.org/10.1007/BF01874789
Bdliya, B. S., & Langerfeld, E. (2005). A semi-selective medium for detection, isolation and enumeration of Erwinia carotovora ssp. Carotovora from plant materials and soil. Tropical Science, 45(2), 90–96. https://doi.org/10.1002/ts.56
Bhat, K., Masood, S., Bhat, N., Bhat, M. A., Razvi, S., Mir, M., Akhtar, S., Wani, N., & Habib, M. (2010). Current status of post harvest soft rot in vegetables: A review. Asian Journal of Plant Sciences, 9(4), 200–208. https://doi.org/10.3923/ajps.2010.200.208
Bonas, U., Schulte, R., Fenselau, S., Minsavage, G. V., Staskawicz, B. J., & Stall, R. E. (1991). Isolation of a gene cluster from Xanthomonas campestris pv. Vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Molecular Plant-Microbe Interactions, 4(1), 81–88. https://doi.org/10.1094/mpmi-4-081
Brisse, S., Grimont, F., & Grimont, P. A. D. (2006). The genus Klebsiella. In M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, & E. Stackebrandt (Eds.), The Prokaryotes: Volume 6: Proteobacteria: Gamma Subclass (pp. 159–196). Springer New York. https://doi.org/10.1007/0-387-30746-X_8
Brown, C., & Seidler, R. J. (1973). Potential pathogens in the environment: Klebsiella pneumoniae, a taxonomic and ecological enigma. Applied Microbiology, 25(6), 900–904. https://doi.org/10.1128/AEM.25.6.900-904.1973
Byrd, A. L., & Segre, J. A. (2016). Adapting Koch’s postulates. Science, 351(6270), 224–226. https://doi.org/10.1126/science.aad6753
Chandrashekar, B. S., Prasannakumar, M. K., Puneeth, M. E., Teli, K., Priyanka, K., Mahesh, H. B., & Desai, R. U. (2018). First report of bacterial soft rot of carrot caused by Klebsiella variicola in India. New Disease Reports, 37, Article 21. https://doi.org/10.5197/j.2044-0588.2018.037.021
Charkowski, A.O. (2007). The soft rot Erwinia. In S. S. Gnanamanickam (Ed.), Plant-Associated Bacteria (pp. 423-505). Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-4538-7_13
Charkowski, A. O. (2018). The Changing Face of Bacterial Soft-Rot Diseases. Annual Review of Phytopathology, 56(1), 269–288. https://doi.org/10.1146/annurev-phyto-080417-045906
Charkowski, A., Blanco, C., Condemine, G., Expert, D., Franza, T., Hayes, C., Hugouvieux-Cotte-Pattat, N., Solanilla, E. L., 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., Yedidia, I. (2012). The role of secretion systems and small molecules in soft-rot enterobacteriaceae pathogenicity. Annual Review of Phytopathology, 50(1), 425–449. https://doi.org/10.1146/annurev-phyto-081211-173013
Charkowski, A. O., Lind, J., & Rubio-Salazar, I. (2014). Genomics of plant-associated bacteria: The soft rot enterobacteriaceae. In D. C. Gross, A. Lichens-Park, & C. Kole, (Eds.), Genomics of plant-associated bacteria (pp. 37–58). Springer. https://doi.org/10.1007/978-3-642-55378-3_2
Chinchilla, C., Gonzales, L., & Morales, F. (1979). Purdrición bacteriana del cogollo de la piña en Costa Rica. Agronomía Costarricense, 3(2), 183–185.
Choi, O., & Kim, J. (2013). Pectobacterium carotovorum subsp. Brasiliense Causing Soft Rot on Paprika in Korea. Journal of Phytopathology, 161(2), 125–127. https://doi.org/10.1111/jph.12022
Czajkowski, R., Pérombelon, M. C. M., Jafra, S., Lojkowska, E., Potrykus, M., van der Wolf, J. M., & Sledz, W. (2015). Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: A review. Annals of Applied Biology, 166(1), 18–38. https://doi.org/10.1111/aab.12166
Davidsson, P. R., Kariola, T., Niemi, O., & Palva, T. (2013). Pathogenicity of and plant immunity to soft rot pectobacteria. Frontiers in Plant Science, 4, Article 191. https://doi.org/10.3389/fpls.2013.00191
Duarte, V., Boer, S. H. D., 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(3), 535–545. https://doi.org/10.1111/j.1365-2672.2004.02173.x
Estrada, R. S. G., Reyes, C. J., Fasio, J. A. C., Molar, R. A., Zequera, I. M., & Rangel, M. D. M. (2000). Marchitez bacteriana en chile bell causada por Erwinia carotovora subsp carotovora. Revista Mexicana de Fitopatología, 18(2), 120–124.
Etalo, D. W., Stulemeijer, I. J. E., Esse, H. P. van, de Vos, R. C. H., Bouwmeester, H. J., & Joosten, M. H. A. J. (2013). System-Wide Hypersensitive Response-Associated Transcriptome and Metabolome Reprogramming in Tomato. Plant Physiology, 162(3), 1599–1617. https://doi.org/10.1104/pp.113.217471
Fan, H. C., Zeng, L., Yang, P. W., Guo, Z. X., & Bai, T. T. (2016). First report of banana soft rot caused by Klebsiella variicola in China. Plant Disease, 100(2), 517–517. https://doi.org/10.1094/PDIS-05-15-0586-PDN
Feng, F., & Zhou, J. M. (2012). Plant–bacterial pathogen interactions mediated by type III effectors. Current Opinion in Plant Biology, 15(4), 469–476. https://doi.org/10.1016/j.pbi.2012.03.004
Fontecha, G. (2003). Análisis comparativo de las comunidades de procariotas intestinales de Rothschildia lebeau (Lepidoptera) mediante los polimorfismos en los fragmentos terminales de restricción (T-RFLP) del gen ARNr 16S [Tesis de Maestría no publicada]. Universidad de Costa Rica.
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(2), 381–391. https://doi.org/10.1099/ijs.0.02423-0
Gillis, A., Santana, M. A., Rodríguez, M., & Romay, G. (2017). First Report of Bell Pepper Soft-Rot Caused by Pectobacterium carotovorum subsp. Brasiliense in Venezuela. Plant Disease, 101(9), 1671–1671. https://doi.org/10.1094/PDIS-03-17-0361-PDN
Govrin, E. M., & Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology, 10(13), 751–757. https://doi.org/10.1016/S0960-9822(00)00560-1
Gupta, R., Lee, S. E., Agrawal, G. K., Rakwal, R., Park, S., Wang, Y., & Kim, S. T. (2015). Understanding the plant-pathogen interactions in the context of proteomics-generated apoplastic proteins inventory. Frontiers in Plant Science, 6, Article 352. https://doi.org/10.3389/fpls.2015.00352
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98. https://doi.org/10.14601/Phytopathol_Mediterr-14998u1.29
Hélias, V., Hamon, P., Huchet, E., Wolf, J. V. D., & Andrivon, D. (2012). Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya. Plant Pathology, 61(2), 339–345. https://doi.org/10.1111/j.1365-3059.2011.02508.x
Herrera, J., & González, L. (1977). Development and control of potato blackleg, caused by Erwinia carotovora var. Atroseptica, in Costa Rica. Agronomía Costarricense, 1(2), 161–163.
Huang, H. E., Ger, M. J., Yip, M. K., Chen, C. Y., Pandey, A. K., & Feng, T. Y. (2004). A hypersensitive response was induced by virulent bacteria in transgenic tobacco plants overexpressing a plant ferredoxin-like protein (PFLP). Physiological and Molecular Plant Pathology, 64(2), 103–110. https://doi.org/10.1016/j.pmpp.2004.05.005
Hugouvieux-Cotte-Pattat, N., Condemine, G., & Shevchik, V. E. (2014). Bacterial pectate lyases, structural and functional diversity. Environmental Microbiology Reports, 6(5), 427–440. https://doi.org/10.1111/1758-2229.12166
Izard, D., Ferragut, C., Gavini, F., Kersters, K., De Ley, J., & Leclerc, H. (1981). Klebsiella terrigena, a New Species from Soil and Water. International Journal of Systematic Bacteriology, 31(2), 116–127. https://doi.org/10.1099/00207713-31-2-116
Jaramillo, A., Huertas, C. A., & Gómez, E. D. (2016). First Report of Bacterial Stem Rot of Tomatoes Caused by Pectobacterium carotovorum subsp. Brasiliense in Colombia. Plant Disease, 101(5), 830. https://doi.org/10.1094/PDIS-08-16-1184-PDN
Jensen, M. A., Webster, J. A., & Straus, N. (1993). Rapid identification of bacteria on the basis of polymerase chain reaction-amplified ribosomal DNA spacer polymorphisms. Applied and Environmental Microbiology, 59(4), 945–952. https://doi.org/10.1128/AEM.59.4.945-952.1993
Kim, J. H., Joen, Y. H., Kim, S. G., & Kim, Y. H. (2007). First report on bacterial soft rot of graft-cactus Chamaecereus silvestrii caused by Pectobacterium carotovorum subsp. Carotovorum in Korea. The Plant Pathology Journal, 23(4), 314-317. https://doi.org/10.5423/PPJ.2007.23.4.314
Kim, H. S., Thammarat, P., Lommel, S. A., Hogan, C. S., & Charkowski, A. O. (2011). Pectobacterium carotovorum Elicits Plant Cell Death with DspE/F but the P. carotovorum DspE Does Not Suppress Callose or Induce Expression of Plant Genes Early in Plant–Microbe Interactions. Molecular Plant-Microbe Interactions, 24(7), 773–786. https://doi.org/10.1094/MPMI-06-10-0143
Klement, Z. (1963). Rapid detection of the pathogenicity of phytopathogenic pseudomonads. Nature, 199, 299–300. https://doi.org/10.1038/199299b0
Klement, Z., & Goodman, R. (1967). The hypersensitive reaction to infection by bacterial plant pathogens. Annual Review of Phytopathology, 5(1), 17-44. https://doi.org/10.1146/annurev.py.05.090167.000313
Knittel, M. D., Seidler, R. J., Eby, C., & Cabe, L. M. (1977). Colonization of the botanical environment by Klebsiella isolates of pathogenic origin. Applied and Environmental Microbiology, 34(5), 557–563. https://doi.org/10.1128/AEM.34.5.557-563.1977
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870–1874. https://doi.org/10.1093/molbev/msw054
Kushalappa, A. C., Yogendra, K. N., & Karre, S. (2016). Plant innate immune response: qualitative and quantitative resistance. Critical Reviews in Plant Sciences, 35(1), 38–55. https://doi.org/10.1080/07352689.2016.1148980
Lane, D. (1991). 16S/23S rRNA sequencing. In E. Stackebrandt, & M. Goodfellow (Eds.), Nucleic acid techniques in bacterial systematics (pp. 115-175). John Wiley & Sons, Inc.
Ma, B., Hibbing, M. E., Kim, H. S., Reedy, R. M., Yedidia, I., Breuer, J., Breuer, J., Glasner, J. D., Perna, N. T., & Kelman, A. (2007). Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology, 97(9), 1150–1163. https://doi.org/10.1094/PHYTO-97-9-1150
McFarland, J. (1907). The nephelometer: An instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. Journal of the American Medical Association, 49(14), 1176–1178. https://doi.org/10.1001/jama.1907.25320140022001f
Meng, X., Chai, A., Shi, Y., Xie, X., Ma, Z., & Li, B. (2016). Emergence of bacterial soft rot in cucumber caused by Pectobacterium carotovorum subsp. Brasiliense in China. Plant Disease, 101(2), 279-287. https://doi.org/10.1094/PDIS-05-16-0763-RE
Nabhan, S., Boer, S. H. D., 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(4), 904–913. https://doi.org/10.1111/j.1365-2672.2012.05383.x
Ngadze, E., Coutinho, T. A., & van der Waals, J. E. (2010). First Report of Soft Rot of Potatoes Caused by Dickeya dadantii in Zimbabwe. Plant Disease, 94(10), 1263–1263. https://doi.org/10.1094/PDIS-05-10-0361
Nguyen-the, C., & Carlin, F. (1994). The microbiology of minimally processed fresh fruits and vegetables. Critical Reviews in Food Science & Nutrition, 34(4), 371–401. https://doi.org/10.1080/10408399409527668
Perombelon, M. C., & Kelman, A. (1980). Ecology of the soft-rot Erwinias. Annual Review of Phytopathology, 18(1), 361–387. https://doi.org/10.1146/annurev.py.18.090180.002045
Pitman, A. R., Harrow, S. A., & Visnovsky, S. B. (2010). Genetic characterisation of Pectobacterium wasabiae causing soft rot disease of potato in New Zealand. European Journal of Plant Pathology, 126(3), 423–435. https://doi.org/10.1007/s10658-009-9551-y
Pitman, A. R., Wright, P. J., Galbraith, M. D., & Harrow, S. A. (2008). Biochemical and genetic diversity of pectolytic enterobacteria causing soft rot disease of potatoes in New Zealand. Australasian Plant Pathology, 37(6), 559–568. https://doi.org/10.1071/AP08056
Pu, X. M., Zhou, J. N., Lin, B. R., & Shen, H. F. (2012). First report of bacterial foot rot of rice caused by a Dickeya zeae in China. Plant Disease, 96(12), 1818–1818. https://doi.org/10.1094/PDIS-03-12-0315-PDN
Ritchie, D. (2000). Bacterial spot of pepper and tomato. The Plant Health Instructor. The American Phytopathological Society. https://doi.org/10.1094. PHI-I-2000-1027-01.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology, 61(3), 539–542. https://doi.org/10.1093/sysbio/sys029
Sánchez, K. R., Zúñiga, O. C., Meneses, M. B., & González, A. Q. (2019). Etiología de las pudriciones en el tallo de Hylocereus costaricensis, provocadas por Enterobacter hormaechei, en Costa Rica. Agronomía Costarricense, 43(2), 61–73. https://doi.org/10.15517/rac.v43i2.37949
Schaad, N. W., Jones, J. B., & Chun, W. (2001). Laboratory guide for the identification of plant pathogenic bacteria. American Phytopathological Society Press.
Singh, J., & Kaur, L. (2016). Advances in potato chemistry and technology (2nd ed.). Academic press.
Staats, M., van Baarlen, P., & van Kan, J. A. L. (2005). Molecular Phylogeny of the Plant Pathogenic Genus Botrytis and the Evolution of Host Specificity. Molecular Biology and Evolution, 22(2), 333–346. https://doi.org/10.1093/molbev/msi020
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(1), 17–30. https://doi.org/10.1046/j.1364-3703.2003.00149.x
Umesha, S., Richardson, P. A., Kong, P., & Hong, C. X. (2008). A novel indicator plant to test the hypersensitivity of phytopathogenic bacteria. Journal of Microbiological Methods, 72(1), 95–97. https://doi.org/10.1016/j.mimet.2007.11.002
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(2), 175–185. https://doi.org/10.1007/s10658-009-9531-2
Volcy, C. (2008). Genesis and evolution of Koch postulates and their relationship with phytopathology. A review. Agronomía Colombiana, 26(1), 107-115.
Waleron, M., Waleron, K., & Lojkowska, E. (2015). First Report of Pectobacterium carotovorum subsp. Brasiliense causing soft rot on potato and other vegetables in Poland. Plant Disease, 99(9), 1271–1271. https://doi.org/10.1094/PDIS-02-15-0180-PDN
Wei-Salas, S., & Durán-Quirós, A. (2015). Characterization of land use in the main agricultural areas of the Major Metropolitan Area of Costa Rica. Agronomía Costarricense, 39(1), 151–160.
Williams, B., Kabbage, M., Kim, H.-J., Britt, R., & Dickman, M. B. (2011). Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLOS Pathogens, 7(6), e1002107. https://doi.org/10.1371/journal.ppat.1002107
Wright, P., Triggs, C., & Burge, G. (2005). Control of bacterial soft rot of calla (Zantedeschia spp.) by pathogen exclusion, elimination and removal. New Zealand Journal of Crop and Horticultural Science, 33(2), 117–123. https://doi.org/10.1080/01140671.2005.9514340
Zhang, J., Shen, H., Pu, X., Lin, B., & Hu, J. (2014). Identification of Dickeya zeae as a Causal Agent of Bacterial Soft Rot in Banana in China. Plant Disease, 98(4), 436–442. https://doi.org/10.1094/PDIS-07-13-0711-RE
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
1. Proposed policy for open access journals
Authors who publish in this journal accept the following conditions:
a. Authors retain the copyright and assign to the journal the right to the first publication, with the work registered under the attribution, non-commercial and no-derivative license from Creative Commons, which allows third parties to use what has been published as long as they mention the authorship of the work and upon first publication in this journal, the work may not be used for commercial purposes and the publications may not be used to remix, transform or create another work.
b. Authors may enter into additional independent contractual arrangements for the non-exclusive distribution of the version of the article published in this journal (e.g., including it in an institutional repository or publishing it in a book) provided that they clearly indicate that the work was first published in this journal.
c. Authors are permitted and encouraged to publish their work on the Internet (e.g. on institutional or personal pages) before and during the review and publication process, as it may lead to productive exchanges and faster and wider dissemination of published work (see The Effect of Open Access).