Skip to main content
SpringerLink
Log in

Genotypic and phenotypic characterization of the European A2 isolates of Phytophthora ramorum

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Phytophthora ramorum, a recently described North American and European pathogen, has three clonal lineages. The NA1 and NA2 lineages are found in North American forests and nurseries, while the EU1 lineage appears mainly in European nurseries. P. ramorum is heterothallic, having two mating types A1 and A2. All NA1 and NA2 isolates are of A2 mating type. When first collected, all EU1 isolates were of A1 mating type, with the exception of one A2 isolate collected in Belgium in 2002. Screening 410 other Belgian isolates for mating type revealed two additional EU1-A2 isolates collected in 2002 and 2003. PCR-RFLP, AFLP and SSR markers were used to determine the nature of the mating type change. The three isolates show no indications of sexual recombination or mitotic crossing over, indicating that mutation or mitotic gene conversion is the most likely explanation for the mating type change. We compared the pathogenicity and sporulation characteristics of the EU1-A2 isolates to those of EU1-A1 and NA1-A2 isolates on four host plants. Despite small differences in pathogenicity on some hosts, the EU1-A2 isolates were similarly aggressive to each other and to the EU1-A1 isolates and more aggressive than the NA1-A2 isolates. Sporulation characteristics were also comparable among EU1-A2 isolates and between EU1-A1 and EU1-A2 isolates, except for EU1-A2 isolate BBA 26/02. The limited genotypic and phenotypic differences between EU1-A2 isolates probably evolved after the mating type change, which may have occurred several years before the isolates were detected. There are strong indications that the EU1-A2 population has been eradicated from Belgium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Boutet, X., Laurent, F., & Chandelier, A. (2009). Influence of the medium-solidifying agent, the nutrient, and the genotype on the production of oogonia by Phytophthora ramorum in vitro. Mycological Research, 113, 110–116.

    Article  PubMed  Google Scholar 

  • Boutet, X., Vercauteren, A., Heungens, K., Laurent, F., & Chandelier, A. (2010). Oospore progenies from Phytophthora ramorum. Fungal Biology, 114, 369–378.

    Article  Google Scholar 

  • Brasier, C. M. (2003). Sudden Oak Death: Phytophthora ramorum exhibits transatlantic differences. Mycological Research, 107, 258–259.

    Article  PubMed  Google Scholar 

  • Brasier, C. M., & Kirk, S. (2004). Production of oogonia by Phytophthora ramorum in vitro. Mycological Research, 108, 823–827.

    Article  PubMed  Google Scholar 

  • Brasier, C. M., Rose, J., Kirk, S., Denman, S., & Webber, J. (2006). Comparative host range and aggressiveness of Phytophthora ramorum and Phytophthora kernoviae sp. nov. on North American and European trees. In S. J. Frankel, P. J. Shea, & M. I. Haverty (Eds.), Proceedings of the Sudden Oak Death second science symposium: The state of our knowledge. January 18–21, 2005, Monterey, CA. Gen. Tech. Rep. PSW-GTR-196 (pp. 109–111). Albany: US Department of Agriculture, Forest Service, Pacific Southwest Research Station.

    Google Scholar 

  • De Dobbelaere, I., Vercauteren, A., Speybroeck, N., Berkvens, D., Van Bockstaele, E., Maes, M., et al. (2010). Effect of host factors on the susceptibility of Rhododendron to Phytophthora ramorum. Plant Pathology, 59, 301–312.

    Article  Google Scholar 

  • DEFRA Science and Research. (2004). Comparison of Phytophthora ramorum (Sudden Oak Death) populations from Europe and USA in support of pest risk assessment, management and policy (PH0192) (http://randd.defra.gov.uk/Document.aspx?Document=PH0192_2458_FRP.pdf).

  • Denman, S., Kirk, S. A., Brasier, C. M., & Webber, J. F. (2005). In vitro leaf inoculation studies as an indication of tree foliage susceptibility to Phytophthora ramorum in the UK. Plant Pathology, 54, 512–521.

    Article  Google Scholar 

  • Elliott, M., Shamoun, S. F., Sumampong, G., James, D., Masri, S., & Varga, A. (2009). Effects of several fungicides on mycelial growth, chlamydospore formation, and zoospore germination of Phytophthora ramorum. Canadian Journal of Plant Pathology, 31, 135–136.

    Article  Google Scholar 

  • Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. St Paul: American Phytopathological Society.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grünwald, N. J., Goss, E. M., & Press, C. M. (2008a). Phytophthora ramorum: a pathogen with a remarkably wide host range causing Sudden Oak Death on oaks and ramorum blight on woody ornamentals. Molecular Plant Pathology, 9, 729–740.

    Article  Google Scholar 

  • Grünwald, N. J., Kitner, M., McDonald, V., & Goss, E. M. (2008b). Susceptibility in Viburnum to Phytophthora ramorum. Plant Disease, 92, 210–214.

    Article  Google Scholar 

  • Grünwald, N. J., Goss, E. M., Larsen, M. M., Press, C. M., McDonald, V. T., Blomquist, C. L., et al. (2008c). First report of the European lineage of Phytophthora ramorum on viburnum and Osmanthus spp. in a California nursery. Plant Disease, 92, 314.

    Article  Google Scholar 

  • Grünwald, N. J., Goss, E. M., Ivors, K., Garbelotto, M., Martin, F. N., Prospero, S., et al. (2009). Standardizing the nomenclature for clonal lineages of the Sudden Oak Death pathogen, Phytophthora ramorum. Phytopathology, 99, 792–795.

    Article  PubMed  Google Scholar 

  • Hansen, E. M., Reeser, P. W., Sutton, W., Winton, L. M., & Osterbauer, N. (2003). First report of A1 mating type of Phytophthora ramorum in North America. Plant Disease, 87, 1267.

    Article  Google Scholar 

  • Hüberli, D., Harnik, T., Meshiry, M., Miles, L., & Garbelotto, M. (2006). Phenotypic variation among Phytophthora ramorum isolates from California and Oregon. In S. J. Frankel, P. J. Shea, & M. I. Haverty (Eds.), Proceedings of the Sudden Oak Death second science symposium: The state of our knowledge. January 18–21, 2005, Monterey, CA. Gen. Tech. Rep. PSW-GTR-196 (pp. 131–134). Albany: US Department of Agriculture, Forest Service, Pacific Southwest Research Station.

    Google Scholar 

  • Ivors, K. L., Hayden, K. J., Bonants, P. J., Rizzo, D. M., & Garbelotto, M. (2004). AFLP and phylogenetic analyses of North American and European populations of Phytophthora ramorum. Mycological Research, 108, 378–392.

    Article  PubMed  CAS  Google Scholar 

  • Ivors, K. L., Garbelotto, M., Vries, I. D. E., Ruyter-Spira, C., Te Hekkert, B., Rosenzweig, N., et al. (2006). Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Molecular Ecology, 15, 1493–1505.

    Article  PubMed  CAS  Google Scholar 

  • Judelson, H. S. (1996). Chromosomal heteromorphism linked to the mating type locus of the oomycete Phytophthora infestans. Molecular & General Genetics, 252, 155–161.

    Article  CAS  Google Scholar 

  • Kroon, L. P. N. M., Verstappen, E. C. P., Kox, L. F. F., Flier, W. G., & Bonants, P. J. M. (2004). A rapid diagnostic test to distinguish between American and European populations of Phytophthora ramorum. Phytopathology, 94, 613–620.

    Article  PubMed  CAS  Google Scholar 

  • Martin, F. N. (2008). Mitochondrial haplotype determination in the oomycete plant pathogen Phytophthora ramorum. Current Genetics, 54, 23–34.

    Article  PubMed  CAS  Google Scholar 

  • Mascheretti, S., Croucher, P. J. P., Vettraino, A., Prospero, S., & Garbelotto, M. (2008). Reconstruction of the Sudden Oak Death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum. Molecular Ecology, 17, 2755–2768.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, V. T., Grunwald, N. J., & Linderman, R. G. (2006). Evaluation of infection potential and sporulation of Phytophthora ramorum on five Rhododendron cultivars. Phytopathology, 96, S75.

    Google Scholar 

  • Meentemeyer, R. K., Rank, N. E., Shoemaker, D. A., Oneal, C. B., Wickland, A. C., Frangioso, K. M., et al. (2008). Impact of Sudden Oak Death on tree mortality in the Big Sur ecoregion of California. Biological Invasions, 10, 1243–1255.

    Article  Google Scholar 

  • Prospero, S., Grünwald, N. J., Winton, L. M., & Hansen, E. M. (2009). Migration patterns of the emerging plant pathogen Phytophthora ramorum on the West Coast of the United States of America. Phytopathology, 99, 739–749.

    Article  PubMed  CAS  Google Scholar 

  • RAPRA. (2009). Risk Analysis of Phytophthora ramorum (FP6 Project 502672) (http://randd.defra.gov.uk/Document.aspx?Document=PH0192_2458_FRP.pdf).

  • Rizzo, D. M., Garbelotto, M., Davidson, J. M., Slaughter, G. W., & Koike, S. T. (2002). Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease, 86, 205–214.

    Article  Google Scholar 

  • Suassuna, N. D., Maffia, L. A., & Mizubuti, E. S. G. (2004). Aggressiveness and host specificity of Brazilian isolates of Phytophthora infestans. Plant Pathology, 53, 405–413.

    Article  Google Scholar 

  • Tooley, P. W., Kyde, K. L., & Englander, L. (2004). Susceptibility of selected ericaceous ornamental host species to Phytophthora ramorum. Plant Disease, 88, 993–999.

    Article  Google Scholar 

  • Tracy, D. R. (2009). Phytophthora ramorum and Phytophthora kernoviae: the woodland perspective. EPPO Bulletin, 39, 161–167.

    Article  Google Scholar 

  • Vercauteren, A., De Dobbelaere, I., Grünwald, N. J., Bonants, P., Van Bockstaele, E., Maes, M., et al. (2010). Clonal expansion of the Belgian Phytophthora ramorum populations based on new microsatellite markers. Molecular Ecology, 19, 92–107.

    Article  PubMed  CAS  Google Scholar 

  • Werres, S., & De Merlier, D. (2003). First detection of Phytophthora ramorum mating type A2 in Europe. Plant Disease, 87, 1266.

    Article  Google Scholar 

  • Werres, S., & Kaminski, K. (2005). Characterisation of European and North American Phytophthora ramorum isolates due to their morphology and mating behaviour in vitro with heterothallic Phytophthora species. Mycological Research, 109, 860–871.

    Article  PubMed  Google Scholar 

  • Werres, S., Marwitz, R., Veld, W. A. M. I., De Cock, A. W. A. M., Bonants, P. J. M., De Weerdt, M., et al. (2001). Phytophthora ramorum sp nov., a new pathogen on Rhododendron and Viburnum. Mycological Research, 105, 1155–1165.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Wannes Voorend and Tineke Van Vooren for technical assistance. We are grateful to Xavier Boutet and Anne Chandelier from the CRA-W for conducting the mating type assays of the Walloon isolates. We thank Peter Bonants for providing P. ramorum isolates PRI549, PRI480 and PRI483. Funding for this research was provided by the Belgian Federal Public Service (FPS) “Health, Food Chain Safety and Environment” (project RT-05/04-PHYRAM1) and the Belgian Plant Protection Service—FAVV (agreement 10-ILVOCRA-Planten). We thank Miriam Levenson for English language editing.

Author information

Authors and Affiliations

  1. Plant Sciences Unit - Crop Protection, Institute for Agricultural and Fisheries Research (ILVO), Burg. Van Gansberghelaan 96 bus 2, 9820, Merelbeke, Belgium

    Annelies Vercauteren, Isabelle De Dobbelaere, Erik Van Bockstaele, Martine Maes & Kurt Heungens

  2. Department of Plant Production, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, 9000, Ghent, Belgium

    Annelies Vercauteren, Isabelle De Dobbelaere & Erik Van Bockstaele

Authors
  1. Annelies Vercauteren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle De Dobbelaere
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erik Van Bockstaele
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martine Maes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kurt Heungens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kurt Heungens.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vercauteren, A., De Dobbelaere, I., Van Bockstaele, E. et al. Genotypic and phenotypic characterization of the European A2 isolates of Phytophthora ramorum . Eur J Plant Pathol 129, 621–635 (2011). https://doi.org/10.1007/s10658-010-9727-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-010-9727-5

Keywords

Search

Navigation