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Cross pathogenicity of Fusarium oxysporum isolated from peppers

  • Carlos Alfonso López-Orona
  • Sergio Hernández-Verdugo
  • Sixto Velarde-Félix
  • José Antonio Garzón-Tiznado
  • Ousmane Sy
  • Jesús Enrique Retes-ManjarrezEmail author
Article
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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.

Keywords

Cucurbitaceae Fol races Fusarium oxysporum Host specificity SIX genes Solanaceae 

Notes

Compliance with ethical standards

No part of the manuscript has been previously published or is in consideration for publication in another journal.

Conflict of interest

The authors declare that they have no conflict of interest. All authors are in complete agreement for the submission of the manuscript.

Supplementary material

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ESM 1 (DOCX 1891 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. 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.
  3. 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
  4. 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.
  5. Booth, C. (1971). The Genus Fusarium. Commonwealth mycological institute. Surrey: Kew.Google Scholar
  6. 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
  7. 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.Google Scholar
  8. 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.CrossRefGoogle Scholar
  9. Davis, D. (1966). Cross-infection in Fusarium wilt diseases. Phytopathology, 56, 825–828.Google Scholar
  10. 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.CrossRefGoogle Scholar
  11. Flor, H. H. (1971). Current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275–296.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.Google Scholar
  15. 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.CrossRefGoogle Scholar
  16. Gordon, T. R., & Martyn, R. D. (1997). The evolutionary biology of Fusarium oxysporum. Annual Review of Phytopathology, 35, 111–128.CrossRefGoogle Scholar
  17. Grattidge, R., & O’Brien, R. G. (1982). Occurrence of a third race of Fusarium wilt of tomatoes in Queensland. Plant Disease, 66, 165–166.CrossRefGoogle Scholar
  18. Hawksworth, D. L., Kirk, P. M., Sutton, B. C., & Pegler, D. N. (1995). Dictionary of the Fungi. Wallingford: CAB International.Google Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. Jarvis, W. R. (1989). Managing diseases in greenhouse crops. Plant Disease, 73, 190–194.CrossRefGoogle Scholar
  25. 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.Google Scholar
  26. Jones, J. B., Jones, J. P., Stall, R. E., & Zitter, T. A. (1991). Compendium of Tomato Diseases. St. Paul: American Phytopathological Society.Google Scholar
  27. 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
  28. 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.CrossRefGoogle Scholar
  29. Kistler, H. C. (1997). Genetic diversity in the plant-pathogenic fungus Fusarium oxysporum. Phytopathology, 87, 474–479.CrossRefGoogle Scholar
  30. Leach, J. G., & Currence, T. M. (1938). Fusarium wilt of muskmelon in Minnesota. Minnesota Agricultural Experiment Station Bulletin, 129, 32.Google Scholar
  31. Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing. 388 p.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.Google Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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
  39. McGovern, R. J. (2015). Management of tomato diseases caused by Fusarium oxysporum. Crop Protection.  https://doi.org/10.1016/j.cropro.2015.02.021.
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Michielse, C. B., & Rep, M. (2009). Pathogen profile update: Fusarium oxysporum. Molecular Plant Pathology, 10, 311–324.CrossRefGoogle Scholar
  43. Nelson, P. E. (1991). History of Fusarium systematics. Phytopathology, 81, 1045–1048.Google Scholar
  44. 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.CrossRefGoogle Scholar
  45. O’Donnell, K., & Cigelnik, E. (1999). A DNA sequenced-based phylogenetic structure for the Fusarium oxysporum complex. Phytoparasitica, 27, 69.Google Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Owen, J. H. (1955). Fusarium wilt of cucumber. Phytopathology, 45, 435–439.Google Scholar
  49. Owen, J. H. (1956). Cucumber wilt, caused by Fusarium oxysporum f. Sp. cucumerinum. N. f. Phytopathology, 46, 153–157.Google Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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.Google Scholar
  54. 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.CrossRefGoogle Scholar
  55. SAS Institute. (1999). SAS/STAT. User’s Guide. Version 8, Vol. 1–5. Cary: SAS Publishing 3848 p.Google Scholar
  56. Sites, W., & Marshall, J. C. (2004). Operational criteria for delimiting species. Annual Review of Phytopathology, 35, 199–277.Google Scholar
  57. Snyder, W. C., & Hansen, H. N. (1940). The species concept in Fusarium. American Journal of Botany, 27, 64–67.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 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
  68. 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.CrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2019

Authors and Affiliations

  • Carlos Alfonso López-Orona
    • 1
  • Sergio Hernández-Verdugo
    • 1
  • Sixto Velarde-Félix
    • 2
  • José Antonio Garzón-Tiznado
    • 3
  • Ousmane Sy
    • 4
  • Jesús Enrique Retes-Manjarrez
    • 5
    Email author
  1. 1.Facultad de AgronomíaUniversidad Autónoma de SinaloaCuliacánMexico
  2. 2.Campo Experimental Valle de Culiacán-INIFAPCuliacánMexico
  3. 3.Facultad de Ciencias Químico BiológicasUniversidad Autónoma de SinaloaCuliacánMexico
  4. 4.Vilmorin North AmericaHollisterUSA
  5. 5.Universidad Tecnológica de CuliacánCuliacánMexico

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