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Genetic variation and host specificity of Phytophthora citrophthora isolates causing branch cankers in Clementine trees in Spain

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Abstract

Considerable tree losses have been observed during the past few years in Spain due to Phytophthora branch canker of clementines caused by Phytophthora citrophthora. The emergence of this disease led to the speculation that either the pathogen has evolved increasing its aggressiveness or specificity to clementines. A total of 134 isolates of P. citrophthora collected from 2003 to 2005 in 135 citrus orchards in Spain and 22 reference isolates were analyzed genotypically and phenotypically to determine the structure of the population. Genotypic diversity was evaluated by means of Inter-Simple Sequence Repeat (ISSR) markers. Among the phenotypic characteristics examined, sporangial characters, sexual behavior, growth rates and colony morphology of the isolates at different temperatures were studied. The aggressiveness and host-specificity of selected isolates were evaluated by pathogenicity tests on sweet oranges and clementines under field conditions. Phytophthora branch canker of clementines was associated mainly with one genotype (P-1), which included 88% of the isolates obtained from branches. Strains isolated years before the first disease outbreak clustered also with this major genotype, thus it may be considered as a predominant population. Thirteen other minor genotypes were determined, but most contained only one isolate. Although there was wide variation in the morphological and physiological characters, all Phytophthora isolates obtained from branch cankers were sexually sterile and showed a characteristic petalloid colony pattern. As in previous greenhouse studies, pathogenicity tests under field conditions demonstrated that clementines and their hybrids were more susceptible to P. citrophthora than sweet oranges. However, no evidence was found to support the hypothesis that the emergence of the disease was associated with more aggressive or host-specific forms of P. citrophthora.

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References

  • Abu-El Samen, F. M., Secor, G. A., & Gudmestad, N. C. (2003). Variability in virulence among asexual progenies of Phytophthora infestans. Phytopathology, 93, 293–304.

    Article  CAS  Google Scholar 

  • Agustí, M. (2000). Citricultura. Madrid: Ediciones Mundi-Prensa. 416 pp.

    Google Scholar 

  • Alvarez, L. A., Vicent, A., De la Roca, E., Bascón, J., Abad-Campos, P., Armengol, J., et al. (2008a). Branch cankers on citrus trees in Spain caused by Phytophthora citrophthora. Plant Pathology, 57, 84–91.

    Google Scholar 

  • Alvarez, L. A., Vicent, A., Soler, J. M., De la Roca, E., Bascón, J., & García-Jiménez, J. (2008b). Comparison of application methods of systemic fungicides to suppress branch cankers in Clementine trees caused by Phytophthora citrophthora. Plant Disease, 92, 1357–1363.

    Article  CAS  Google Scholar 

  • Alvarez, L. A., Gramaje, D., Abad-Campos, P., & García-Jiménez, J. (2009). Seasonal susceptibility of citrus scions to Phytophthora citrophthora and P. nicotianae and the influence of environmental and host—linked factors on the infection development. European Journal of Plant Pathology, 124, 621–635.

    Article  Google Scholar 

  • Apphia, A. A., Flood, J., Bridge, P. D., & Archer, S. A. (2003). Inter- and intraspecific morphometric variation and characterization of Phytophthora isolates from cocoa. Plant Pathology, 52, 168–180.

    Article  Google Scholar 

  • Bhat, R. G., Colowit, P. M., Tai, T. H., Aradhya, M. K., & Browne, G. T. (2006). Genetic and pathogenic variation in Phytophthora cactorum affecting fruit and nut crops in California. Plant Disease, 90, 161–169.

    Article  CAS  Google Scholar 

  • Bou, F. (1879). Estudio Sobre el Naranjo, Limonero, Cidro y Otros Árboles de la Familia de las Auranciáceas que se Cultivan en la provincia de Castellón. Castellón: Imprenta de Fransisco Segarra.

    Google Scholar 

  • Brasier, C. M. (2008). The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology, 57, 792–808.

    Article  Google Scholar 

  • Cohen, S., Allasia, V., Venard, P., Notter, S., Vernière, C., & Panabières, F. (2003). Intraspecific variation in Phytophthora citrophthora from citrus trees in eastern Corsica. European Journal of Plant Pathology, 109, 791–805.

    Article  CAS  Google Scholar 

  • Cooke, D. E. L., & Duncan, J. M. (1997). Phylogenetic analysis of Phytophthora species based on ITS1 and ITS2 sequences of the ribosomal RNA gene repeat. Mycological Research, 101, 667–677.

    Article  CAS  Google Scholar 

  • Day, J. P., Wattier, R. A. M., Shaw, D. S., & Shattock, R. C. (2004). Phenotypic and genotypic diversity in Phytophthora infestans on potato in Great Britain, 1995–98. Plant Pathology, 53, 303–315.

    Article  Google Scholar 

  • Dice, L. R. (1945). Measures of the amount of ecological association between species. Ecology, 26, 297–302.

    Article  Google Scholar 

  • Eikemo, H., Klemsdal, S. S., Riisberg, I., Bonants, P., Stensvand, A., & Tronsmo, A. M. (2004). Genetic variation between Phytophthora cactorum isolates differing in their ability to cause crown rot in strawberry. Mycological Research, 108, 317–324.

    Article  CAS  PubMed  Google Scholar 

  • Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. St. Paul: APS. 562 pp.

    Google Scholar 

  • Fawcett, H. S. (1936). Citrus diseases and their control. New York: McGraw-Hill. 656 pp.

    Google Scholar 

  • Flier, W. G., Kroon, L. P. N. M., Hermansen, A., van Raaij, H. M. G., Speiser, B., Tamm, L., et al. (2007). Genetic structure and pathogenicity of populations of Phytophthora infestans from organic potato crops in France, Norway, Switzerland and the United Kingdom. Plant Pathology, 56, 562–572.

    Article  CAS  Google Scholar 

  • Goodwin, S. B. (1997). The population genetics of Phytophthora. Phytopathology, 87, 462–473.

    Article  CAS  PubMed  Google Scholar 

  • Hamm, P. B., & Hansen, E. M. (1981). Host specificity of Phytophthora megasperma from douglas-fir, soybean, and alfalfa. Phytopathology, 71, 65–68.

    Article  Google Scholar 

  • Hantula, J., Dusabenyagasani, M., & Hamelin, R. (1996). Random amplified microsatellites (RAMS) a novel method for characterizing genetic variation within fungi. European Journal of Forest Pathology, 26, 159–166.

    Article  Google Scholar 

  • Hantula, J., Lilia, A., & Parikka, P. (1997). Genetic variation and host specificity of Phytophthora cactorum isolated in Europe. Mycological Research, 101, 565–572.

    Article  Google Scholar 

  • Hüberli, D., Tommerup, I. C., Dobrowolski, M. P., Calver, M. C., & Hardy, G. E. St. J. (2001). Phenotypic variation in a clonal lineage of two Phytophthora cinnamomi populations from Western Australia. Mycological Research, 105, 1053–1064.

    Article  Google Scholar 

  • Jeffers, S. N., & Martin, S. B. (1986). Comparison of two media selective for Phytophthora and Pythium species. Plant Disease, 70, 1038–1043.

    Article  Google Scholar 

  • Knapova, G., & Gisi, U. (2002). Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland. Plant Pathology, 51, 641–653.

    Article  Google Scholar 

  • Kumar, S., Tamura, K., & Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150–163.

    Article  CAS  PubMed  Google Scholar 

  • Lamour, K. H., & Hausbeck, M. K. (2000). Mefenoxam insensitivity and the sexual stage of Phytophthora capsici in Michigan cucurbit fields. Phytopathology, 90, 396–400.

    Article  CAS  PubMed  Google Scholar 

  • Lamour, K. H., & Hausbeck, M. K. (2001). The dynamics of mefenoxam insensitivity in a recombining population of Pytophthora capsici characterized with amplified fragment length polymorphism markers. Phytopathology, 91, 553–557.

    Article  CAS  PubMed  Google Scholar 

  • Linde, C., Drenth, A., Kemp, G. H. J., Wingfield, M. J., & von Broembsen, S. L. (1997). Population structure of Phytophthora cinnamomi in South Africa. Phytopathology, 87, 822–827.

    Article  CAS  PubMed  Google Scholar 

  • Madden, L. V. (2001). What are the nonindigenous plant pathogens that threaten U.S. crops and forests? APSnet Feature (October), American Phytopathological Society.

  • Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.

    CAS  PubMed  Google Scholar 

  • McDonald, B. A., & Linde, C. C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.

    Article  CAS  PubMed  Google Scholar 

  • Milgroom, M. G., & Peever, T. L. (2003). Population biology of plant pathogens: the synthesis of plant disease epidemiology and population genetics. Plant Disease, 87, 608–617.

    Article  Google Scholar 

  • Peña, D. (2002). Análisis de datos multivariantes. Madrid: McGraw Hill.

    Google Scholar 

  • Ribeiro, O. (1978). A source book of the genus Phytophthora. Vaduz: Strauss and Cramer. 417 pp.

    Google Scholar 

  • Rullán, J. (1896). Cultivo del naranjo en las Baleares. Soller- España: Imprenta La Sinceridad. 189 pp.

    Google Scholar 

  • Schutte, G. C. (2007). Evaluation of spray programmes for the control of Phytophthora citrophthora on Clementines in the Western Cape. In: CRI annual research report for 2006, pp. 346–354.

  • Stukenbrock, E. H., & McDonald, B. A. (2008). The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology, 46, 75–100.

    Article  CAS  PubMed  Google Scholar 

  • Tuset, J. J. (1977). Contribución al conocimiento del género Phytophthora en España. Anales INIA. Series de Protección Vegetal, 7, 11–106.

    Google Scholar 

  • Tuset, J. J. (1983). La gomosis y podredumbre del cuello de la raíz de nuestros agrios. I: aspectos biológicos y patológicos. Levante Agrícola, 246, 90–96.

    Google Scholar 

  • Urquijo, P., Rodriguez-Sardiña, J., & Santaolalla, G. (1961). Patología vegetal agrícola. Salvat Editores S.A. 780 pp.

  • Vernière, C., Cohen, S., Raffanel, B., Dubois, A., Venard, P., & Panabières, F. (2004). Variability in pathogenicity among Phytophthora spp. isolated from citrus in Corsica. Journal of Phytopathology, 152, 476–483.

    Article  Google Scholar 

  • Vial, A., Latorre, B. A., & Ortúzar, J. (2006). Characterization of Phytophthora citrophthora and P. inundata associated to foot and root rot of citrus trees in Chile. Ciencia e Investigación Agraria, 33, 205–216.

    Google Scholar 

  • Waterhouse, G. M. (1963). Key to the species of Phytophthora de Bary. Mycological Papers, 92, 1–22.

    Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetic. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols, A guide to methods and applications (pp. 315–322). San Diego: Academic.

    Google Scholar 

  • Zietkiewicz, E., Rafalski, A., & Labuda, D. (1994). Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics, 20, 176–183.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Antonio Ippolito (Università di Bari, Italy), Bernardo A. Latorre (Pontificia Universidad Católica, Chile), Frank Panabières (INRA, France) and Juan J. Tuset (IVIA, Spain) for providing reference Phytophthora isolates for this study. We also express our thanks to B.A. Latorre (Pontificia Universidad Católica, Chile), L.W. Timmer (University of Florida, USA) and J.J. Tuset (IVIA, Spain) for critical suggestions upon reviewing the manuscript and to Perfecto Sanz for excellent technical assistance.

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  1. Luis Armando Alvarez

    Present address: Departamento de Sanidad Vegetal, Facultad de Agronomía, Universidad Nacional San Luis Gonzaga de Ica, Panamericana Sur km 299, Ica, Peru

  2. Antonio Vicent

    Present address: Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias (IVIA), 46113, Moncada, Spain

Authors and Affiliations

  1. Instituto Agroforestal Mediterráneo, Universidad Politécnica de Valencia, Camino de Vera s/n, 46022, Valencia, Spain

    Luis Armando Alvarez, Maela León, Paloma Abad-Campos, José García-Jiménez & Antonio Vicent

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  1. Luis Armando Alvarez
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Correspondence to Luis Armando Alvarez.

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Alvarez, L.A., León, M., Abad-Campos, P. et al. Genetic variation and host specificity of Phytophthora citrophthora isolates causing branch cankers in Clementine trees in Spain. Eur J Plant Pathol 129, 103–117 (2011). https://doi.org/10.1007/s10658-010-9696-8

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