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Cross pathogenicity of Fusarium oxysporum isolated from peppers

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Abstract

A new case of Fusarium oxysporum (Fo) causing significant economic losses in pepper (Capsicum annuum) crops in Culiacan, Mexico was recently reported. To fight this newly discovered disease, it was necessary to analyze the host specificity to use this information in an integrated disease management. To achieve that, the host range of 10 strains of Fo collected from diseased pepper plants was checked on the following species: Capsicum annuum, Solanum lycopersicum, Nicotiana tabacum, Nicotiana bethamiana, Solanum melongenea, Phisalis ixocarpa, Cucurbita pepo, Cucumis sativus, Cucumis melo. These 10 strains were also tested on four differential tomato cultivars for Fo f. sp. lycopersici (Fol) races identification. Both assays were repeated twice under growth-chamber conditions. All 10 strains of Fo caused wilting symptoms on each of the species mentioned above, indicating that these strains have a wide host range. During race characterization assays, the typical phenotypic responses displayed by the four differentials ‘Bony Best’, ‘Manapal’, ‘Walter’ and ‘I3R3’ against these 10 strains, suggested that all these strains belong to Fol race 2 (Fol-2). These strains were tested by using PCR technique to detect the SIX genes specific for Fol races and the results indicated also that these strains belong to Fol-2. However, further molecular and vegetative compatibility group studies with these strains most be carry out to corroborate these results. To our knowledge, this is the first cross pathogenicity report of Fo in Solanaceae and Cucurbitaceae crops in Mexico.

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References

  • Baayen, R. P., O’Donnell, K., Bonants, P. J. M., Cigelnik, E., Kroon, L. P. N. M., Roebroeck, J. A., & Waalwijk, C. (2000). Gene genealogies and AFLP analysis in the Fusarium oxysporum complex identify monophyletic and non-monophyletic formae speciales causing wilt and rot disease. Phytopathology, 90, 891–900.

    Article  CAS  PubMed  Google Scholar 

  • Biju, V. C., Fokkens, L., Houterman, P. M., Rep, M., & Cornelissen, B. J. C. (2017). Multiple evolutionary trajectories have led to the emergence of races in Fusarium oxysporum f. Sp. lycopersici. Applied and Environmental Microbiology, 83. https://doi.org/10.1128/AEM.02548-16.

  • Black, L. L. (2003). Fusarium wilt. In K. Perezny, P. D. Roberts, J. F. Murphy, & N. P. Goldberg (Eds.), Compendium of Pepper Diseases (pp. 14–15). St. Paul: APS Press.

    Google Scholar 

  • Boix-Ruíz, A., Gálvez-Patón, L., de Cara-García, M., Palmero-Llamas, D., Camacho-Ferre, F., & Tello-Marquina, J. C. (2014). Comparison of analytical techniques used to identify tomato-pathogenic strains of Fusarium oxysporum. Phytoparasitica, 43, 471–483. https://doi.org/10.1007/s12600-014-0444-z.

  • Booth, C. (1971). The Genus Fusarium. Commonwealth mycological institute. Surrey: Kew.

    Google Scholar 

  • Bouhot, D. (1981). Some aspects of the pathogenic potential in formae speciales and races of Fusarium oxysporum on Cucurbitaceae. In P. E. Nelson, T. A. Toussoun, & R. J. Cook (Eds.), Fusarium: Disease, Biology, and Taxonomy (pp. 318–326). University Park: Pennsylvania State University Press.

    Google Scholar 

  • Cerkauskas, R. F (2017) Etiology and management of Fusarium crown and root rot (Fusarium oxysporum) on greenhouse pepper in Ontario, Canada. Canadian Journal of Plant Pathology, 39(2), 121-132.

  • Collange, B., Navarrete, M., Montfort, F., Mateille, T., Tavoillot, J., Martiny, B., & Tchamitchian, M. (2014). Alternative cropping systems can have contrasting effects on various soil-borne diseases: Relevance of a systemic analysis in vegetable cropping systems. Crop Protection, 55, 7–15.

    Article  Google Scholar 

  • Davis, D. (1966). Cross-infection in Fusarium wilt diseases. Phytopathology, 56, 825–828.

    Google Scholar 

  • Dean, R., Van Kan, J. A., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J., & Foster, G. D. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13, 414–430.

    Article  PubMed  PubMed Central  Google Scholar 

  • Flor, H. H. (1971). Current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275–296.

    Article  Google Scholar 

  • Fourie, G., Steenkamp, E. T., Gordon, T. R., & Viljoen, A. (2009). Evolutionary relationships among the vegetative compatibility groups of Fusarium oxysporum f.Sp. cubense. Applied and Environmental Microbiology, 75, 4770–4781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fourie, G., Steenkamp, E. T., Ploetz, R. C., Gordon, T. R., & Viljoen, A. (2011). Current status of the taxonomic position of Fusarium oxysporum formae specialis cubense within the Fusarium oxysporum complex. Infection, Genetics and Evolution, 11, 533–542.

    Article  CAS  PubMed  Google Scholar 

  • Geiser DM, Jimenez-Gasco MM, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. European Journal of Plant Pathology 110:473–479.

  • Gerlagh, M., & Blok, W. J. (1988). Fusarium oxysporum f. Sp. cucurbitacearum n. f. Embracing all formae speciales of F. oxysporum attacking cucurbitaceous crops. Netherlands Journal of Plant Pathology, 94, 17–31.

    Article  Google Scholar 

  • Gordon, T. R., & Martyn, R. D. (1997). The evolutionary biology of Fusarium oxysporum. Annual Review of Phytopathology, 35, 111–128.

    Article  CAS  PubMed  Google Scholar 

  • Grattidge, R., & O’Brien, R. G. (1982). Occurrence of a third race of Fusarium wilt of tomatoes in Queensland. Plant Disease, 66, 165–166.

    Article  Google Scholar 

  • Hawksworth, D. L., Kirk, P. M., Sutton, B. C., & Pegler, D. N. (1995). Dictionary of the Fungi. Wallingford: CAB International.

    Google Scholar 

  • Hirano, Y., & Arie, T. (2006). PCR-based differentiation of Fusarium oxysporum f. Sp. lycopersici and radicis-lycopersici and races of F. oxysporum f. Sp. lycopersici. Journal of General Plant Pathology, 72, 273–283.

    Article  CAS  Google Scholar 

  • Houterman, P. M., Speijer, D., Dekker, H. L., de Koster, C. G., Cornelissen, B. J. C., & Rep, M. (2007). The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants. Molecular Plant Pathology, 8, 215–221.

    Article  CAS  PubMed  Google Scholar 

  • Houterman, P. M., Cornelissen, B. J. C., & Rep, M. (2008). Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens, 4, e1000061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houterman, P. M., Ma, L., van Ooijen, G., de Vroomen, M. J., Cornelissen, B. J. C., Takken, F. L. W., & Rep, M. (2009). The effector proteinAvr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant Journal, 58, 970–978.

    Article  CAS  PubMed  Google Scholar 

  • Huang, C. C., & Lindhout, P. (1997). Screening for resistance in wild Lycopersicon species to Fusarium oxysporum f. Sp. lycopersici race 1 and race 2. Euphytica, 93, 145–153.

    Article  Google Scholar 

  • Jarvis, W. R. (1989). Managing diseases in greenhouse crops. Plant Disease, 73, 190–194.

    Article  Google Scholar 

  • Jones MM, Black LL. (1992) Response of Capsicum spp. to Fusarium oxysporum f. Sp. capsici and VCG characterization of pathogenic isolates. Phytopathology (Oregon), USA. APS Press; p. 1092.

  • Jones, J. B., Jones, J. P., Stall, R. E., & Zitter, T. A. (1991). Compendium of Tomato Diseases. St. Paul: American Phytopathological Society.

    Google Scholar 

  • Kawai, I., Suzuki, K., & Kawai, K. (1958). On the pathogenicity of the wilt Fusarium of the cucurbitaceous plants and their forms. Shoznoka Agricural Experiment Station Bulletin, 3, 49–68.

    Google Scholar 

  • King, S. R., Davis, A. R., Zhang, X., & Crosby, K. (2010). Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Scientia Horticulturae, 127, 106–111.

    Article  Google Scholar 

  • Kistler, H. C. (1997). Genetic diversity in the plant-pathogenic fungus Fusarium oxysporum. Phytopathology, 87, 474–479.

    Article  CAS  PubMed  Google Scholar 

  • Leach, J. G., & Currence, T. M. (1938). Fusarium wilt of muskmelon in Minnesota. Minnesota Agricultural Experiment Station Bulletin, 129, 32.

    Google Scholar 

  • Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing. 388 p.

  • Lievens, B., Houterman, P. M., & Rep, M. (2009). Effector gene screening allows unambiguous identification of Fusarium oxysporum f. Sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiology Letters, 300, 201–215.

    Article  CAS  PubMed  Google Scholar 

  • Lomas-Cano, T., Palmero-Llamas, D., de Cara-García, M. C., Boix-Ruiz, A., Camacho-Ferre, F., & Tello-Marquina, J. C. (2014). First report of Fusarium oxysporum of sweet pepper seedlings in Almeria, Spain. Plant Disease, 98, 1435.

    Article  CAS  PubMed  Google Scholar 

  • Lomas-Cano, T., Boix-Ruiz, A., de Cara-García, M., Marín-Guirao, J. I., Palmero-Llamas, D., Camacho-Ferre, F., Tello-Marquina, J. C. (2016) Etiological and epidemiological concerns about Pepper root and lower stem rot caused by Fusarium oxysporum f. sp. radicis-capsici f. sp. nova. Phytoparasitica, 44(3), 283-293.

  • Ma, L.-J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M.-J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P. M., Kang, S., Shim, W.-B., Woloshuk, C., Xie, X., Xu, J.-R., Antoniw, J., Baker, S. E., Bluhm, B. H., Breakspear, A., Brown, D. W., Butchko, R. A. E., Chapman, S., Coulson, R., Coutinho, P. M., Danchin, E. G. J., Diener, A., Gale, L. R., Gardiner, D. M., Goff, S., Hammond-Kosack, K. E., Hilburn, K., Hua-Van, A., Jonkers, W., Kazan, K., Kodira, C. D., Koehrsen, M., Kumar, L., Lee, Y.-H., Li, L., Manners, J. M., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S.-Y., Proctor, R. H., Regev, A., Ruiz-Roldan, M. C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D. C., Turgeon, B. G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C. A., Kistler, H. C., & Rep, M. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464, 367–373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marlatt, M. L., Correll, J. C., Kaufmann, P., & Cooper, P. E. (1996). Two genetically distinct populations of Fusarium oxysporum f. Sp. lycopersici race 3 in the United States. Plant Disease, 80, 1336–1342.

    Article  Google Scholar 

  • Martyn, R. D., & McLaughlin, R. J. (1983). Susceptibility of summer squash to the watermelon wilt pathogen (Fusarium oxysporum f. Sp. niveum). Plant Disease, 67, 263–266.

    Article  Google Scholar 

  • Matuo, T., & Yamamoto, I. (1957). On Fusarium oxysporum f. Sp. lagenaria n. f. Causing wilt of Lagenaria vulgaris var. hispida. Transactions of the Mycological Society of Japan, 2, 61–63.

    Google Scholar 

  • McGovern, R. J. (2015). Management of tomato diseases caused by Fusarium oxysporum. Crop Protection. https://doi.org/10.1016/j.cropro.2015.02.021.

  • McMillan, R. T. (1986). Cross pathogenicity studies with isolates of Fusarium oxysporum from either cucumber or watermelon pathogenic to both crop species. Annual Applied Biology, 109, 101–105.

    Article  Google Scholar 

  • Menzies, J. G., Koch, C., & Seywerd, F. (1990). Additions to the host range of Fusarium oxysporum f. Sp. radicis-lycopersici. Plant Disease, 74, 569–572.

    Article  Google Scholar 

  • Michielse, C. B., & Rep, M. (2009). Pathogen profile update: Fusarium oxysporum. Molecular Plant Pathology, 10, 311–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, P. E. (1991). History of Fusarium systematics. Phytopathology, 81, 1045–1048.

    Google Scholar 

  • O’Donnell, K., & Cigelnik, E. (1997). Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution, 7, 103–116.

    Article  PubMed  Google Scholar 

  • O’Donnell, K., & Cigelnik, E. (1999). A DNA sequenced-based phylogenetic structure for the Fusarium oxysporum complex. Phytoparasitica, 27, 69.

    Google Scholar 

  • O’Donnell, K., Kistler, H. C., Cigelnik, E., & Ploetz, R. C. (1998). Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proceding of the National Academy of Sciences USA, 95, 2044–2049.

    Article  Google Scholar 

  • O’Donnell, K., Gueidan, C., Sink, S., Johnston, P. R., Crous, P. W., Glenn, A., Riley, R., Zitomer, N. C., Colyer, P., Waalwijk, C., van der Lee, T., Moretti, A., Kang, S., Kim, H.-S., Geiser, D. M., Juba, J. H., Baayen, R. P., Cromey, M. G., Bithell, S., Sutton, D. A., Skovgaard, K. R., Kistler, P., Elliott, H. C., Davis, M., & Sarver, M. B. A. J. (2009). A twolocus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology, 46, 936–948.

    Article  CAS  PubMed  Google Scholar 

  • Owen, J. H. (1955). Fusarium wilt of cucumber. Phytopathology, 45, 435–439.

    Google Scholar 

  • Owen, J. H. (1956). Cucumber wilt, caused by Fusarium oxysporum f. Sp. cucumerinum. N. f. Phytopathology, 46, 153–157.

    Google Scholar 

  • Pérez-Hernández, A., Serrano-Alonso, Y., Aguilar-Pérez, M. L., Gómez-Uroz, R., & Gómez-Vázquez, J. (2014). Damping-off and root rot of pepper caused by Fusarium oxysporum in Almeria province, Spain. Plant Disease, 98, 1159.

    Article  PubMed  Google Scholar 

  • Rep, M., van der Does, H. C., Meijer, M., van Wijk, R., Houterman, P. M., Dekker, H. L., de Koster, C. G., & Cornelissen, B. J. C. (2004). A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology, 53, 1373–1383.

    Article  CAS  PubMed  Google Scholar 

  • Rep, M., Meijer, M., Houterman, P. M., van der Does, H. C., & Cornelissen, B. J. C. (2005). Fusarium oxysporum evades I-3 mediated resistance without altering the matching avirulence gene. Molecular Plant-Microbe Interactions, 18, 15–23.

    Article  CAS  PubMed  Google Scholar 

  • Rivelli VC. (1989.) A wilt of pepper incited by Fusarium oxysporum f. Sp. capsici formae specialis nova. [M. Sc. Dissertation]. Baton Rouge (Louisiana) Louisiana State University.

  • Rowe, R. C. (1980). Comparative pathogenicity and host ranges of Fusarium oxysporum isolates causing crown and root rot of greenhouse and field-grown tomatoes in North America and Japan. Phytopathology, 70, 1143–1148.

    Article  Google Scholar 

  • SAS Institute. (1999). SAS/STAT. User’s Guide. Version 8, Vol. 1–5. Cary: SAS Publishing 3848 p.

    Google Scholar 

  • Sites, W., & Marshall, J. C. (2004). Operational criteria for delimiting species. Annual Review of Phytopathology, 35, 199–277.

    Google Scholar 

  • Snyder, W. C., & Hansen, H. N. (1940). The species concept in Fusarium. American Journal of Botany, 27, 64–67.

    Article  Google Scholar 

  • Takken, F., & Rep, M. (2010). The arms race between tomato and Fusarium oxysporum. Molecular Plant Pathology, 11, 309–314. https://doi.org/10.1111/j.1364-3703.2009.00605.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbert, D. S., & Fisher, M. C. (2000). Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology, 31, 21–31.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, A., Vagany, V., Jackson, A. C., Harrison, R. J., Rainoni, A., & Clarkson, J. P. (2016). Identification of pathogenicity-related genes in Fusarium oxysporum f. Sp. cepae. Molecular Plant Pathology, 17, 1032–1047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Dam, P., Fokkens, L., Schmidt, S. M., Linmans, J. H. J., Kistler, H. C., Ma, L.-J., & Rep, M. (2016). Effector profiles distinguish formae speciales of Fusarium oxysporum. Environmental Microbiology, 18, 4087–4102.

    Article  CAS  PubMed  Google Scholar 

  • van der Does, H. C., & Rep, M. (2007). Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Molecular Plant-Microbe Interactions, 20, 1175–1182.

    Article  CAS  PubMed  Google Scholar 

  • van der Does, H. C., Lievens, B., Claes, L., Houterman, P. M., Cornelissen, B. J. C., & Rep, M. (2008). The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environmental Microbiology, 10, 1475–1485.

    Article  CAS  PubMed  Google Scholar 

  • Velarde-Félix, S., Ortega-Murrieta, P. F., Fierros-Leyva, G. A., Padilla-Valenzuela, I., Gutiérres-Pérez, E., Rodríguez-Cota, F. G., López-Valenzuela, J. A., Acosta-Gallegos, J. A., & Garzón-Tiznado, J. A. (2015). Identificación molecular y biológica de las razas 0 y 5 de Fusarium oxysporum Schlechtend: Fr f. sp. ciceris (Padwick) Matuo and K. Sato del garbanzo en el noroeste de México. Revista Mexicana de Ciencias Agrícolas, 6, 735–748.

    Article  Google Scholar 

  • Velarde-Félix, S., Garzón-Tiznado, J. A., Hernández-Verdugo, S., López-Orona, C., & Retes-Manjarrez, J. E. (2018). Occurrence of Fusarium oxysporum causing wilt on pepper in Mexico. Canadian Journal of Plant Pathology, 40, 238–247. https://doi.org/10.1080/07060661.2017.1420693.

    Article  Google Scholar 

  • Vlaardingerbroek, I., Beerens, B., Schmidt, S. M., Cornelissen, B. J. C., & Rep, M. (2016). Dispensable chromosomes in Fusarium oxysporum f. Sp lycopersici. Molecular Plant Pathology, 17, 1–12. https://doi.org/10.1111/mpp.12440.

    Article  CAS  Google Scholar 

  • Volin, R. B., & Jones, J. P. (1982). A new race of Fusarium wilt of tomato in Florida and sources of resistance. Proccedings of the Florida State Horticultural Society, 95, 268–270.

    Google Scholar 

  • Webb, K. M., Case, A. J., Brick, M. A., Otto, K., & Schwartz, H. F. (2013). Cross pathogenicity and vegetative compatibility of Fusarium oxysporum isolated from sugar beet. Plant Disease, 97, 1200–1206.

    Article  PubMed  Google Scholar 

  • Zasada, I. A., Halbrendt, J. M., Kokalis-Burelle, N., LaMondia, J., McKenry, M. V., & Noling, J. W. (2010). Managing nematodes without methyl bromide. Annual Review of Phytopathology, 48, 311–328.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, X. G., & Everts, K. L. (2007). Characterization of a regional population of Fusarium oxysporum f. Sp. niveum by race, cross pathogenicity and vegetative compatibility. Phytopathology, 97, 461–469.

    Article  CAS  PubMed  Google Scholar 

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López-Orona, C.A., Hernández-Verdugo, S., Velarde-Félix, S. et al. Cross pathogenicity of Fusarium oxysporum isolated from peppers. Eur J Plant Pathol 154, 1111–1123 (2019). https://doi.org/10.1007/s10658-019-01732-z

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