Presence of Phytophthora species in Swedish Christmas tree plantations

  • Martin PetterssonEmail author
  • John Frampton
  • Jonas Rönnberg
  • May Bente Brurberg
  • Venche Talgø


Phytophthora cryptogea, P. gonapodyides, P. lacustris, P. megasperma, P. plurivora, P. taxon paludosa and an unknown Phytophthora species were isolated from waterways and soil samples in Christmas tree fields in southern Sweden. In addition, P. megasperma was isolated from a diseased Norway spruce (Picea abies) plant from one of the fields in Svalöv. Inoculation tests were sequentially carried out with one isolate from each of the three species P. cryptogea, P. megasperma, and P. plurivora, all known pathogens on conifers. The same three isolates were used to study a few morphological features to confirm the identification, and temperature-growth relationships were carried out to see how well the organisms fit into Swedish climatic conditions. Seedlings of Norway spruce and Nordmann fir (Abies nordmanniana) were inoculated in the roots and the stems. None of the isolates caused extensive root rot under the experimental conditions, but all three species could be re-isolated from both Norway spruce and Nordmann fir. Phytophthora root rot is currently of minor concern for Christmas tree growers in Sweden. However, the Phytophthora isolations from soil and water indicate the presence of this damaging agent, which may lead to future problems.


Phytophthora cryptogea Phytophthora megasperma Phytophthora plurivora Abies Picea Root rot 



The authors are much grateful to Håvard Eikemo, Erling Fløistad and Trude L. Slørstad at NIBIO for their valuable assistance, and to the numerous Christmas tree growers who appreciatively and graciously cooperated in this survey.


  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.CrossRefPubMedGoogle Scholar
  2. Benson, D. M., Hinesley, L. E., Frampton, J., & Parker, K. C. (1997). Evaluation of six Abies spp. to Phytophthora root rot caused by Phytophthora cinnamomi. Biological and Cultural Tests for Control of Plant Diseases, 13, 57.Google Scholar
  3. Brasier, C. M., Hamm, P. B., & Hansen, E. M. (1993). Cultural characters, protein patterns and unusual mating behaviour of Phytophthora gonapodyides isolates from Britain and North America. Mycological Research, 97(11), 1287–1298.CrossRefGoogle Scholar
  4. CANGC (2008). Nursery industry best management practices for Phytophthora ramorum to prevent the introduction or establishment in California nursery operations. Version 1.0. California Association of Nurseries and Garden Centers. Accessed 21 Nov 2018.
  5. Chastagner, G. A., & Benson, D. M. (2000). The Christmas tree: Traditions, production, and diseases. Online. Plant Health Progress, 1, 15. Scholar
  6. Chastagner, G. A., & Riley, K. L. (2010). First report of Phytophthora ramorum infecting California red fir in California. Plant Disease, 94(9), 1170–1170.CrossRefGoogle Scholar
  7. Cleary, M. R., Blomquist, M., Vetukuri, R. R., Bohlenius, H., & Witzell, J. (2017). Susceptibility of common tree species in Sweden to Phytophthora cactorum, P. cambivora and P. plurivora. Forest Pathology, 47(3).
  8. Cleary, M. R., Ghasemkhani, M., Blomquist, M., & Witzell, J. (2016). First report of Phytophthora gonapodyides causing stem canker on European beech (Fagus sylvatica) in southern Sweden. Plant Disease, 100(10), 2174–2175.CrossRefGoogle Scholar
  9. Ersek, T., & Nagy, Z. A. (2008). Species hybrids in the genus Phytophthora with emphasis on the alder pathogen Phytophthora alni: A review. European Journal of Plant Pathology, 122(1), 31–39.CrossRefGoogle Scholar
  10. Ghimire, S. R., Richardson, P. A., Moorman, G. W., Lea-Cox, J. D., Ross, D. S., & Hong, C. X. (2009). An in-situ baiting bioassay for detecting Phytophthora species in irrigation runoff containment basins. Plant Pathology, 58(3), 577–583.CrossRefGoogle Scholar
  11. Hansen, E. M., & Maxwell, D. P. (1991). Species of the Phytophthora megasperma complex. Mycologia, 83(3), 376–381.CrossRefGoogle Scholar
  12. Hansen, E. M., Wilcox, W. F., Reeser, P. W., & Sutton, W. (2009). Phytophthora rosacearum and P. sansomeana, new species segregated from the Phytophthora megasperma "complex". Mycologia, 101(1), 129–135.CrossRefPubMedGoogle Scholar
  13. Hayden, K. J., Hardy, G. E., & Garbelotto, M. (2013). Oomycete diseases. In P. Gonthier & G. Nicolotti (Eds.), Infectious Forest diseases (pp. 519–546). Boston: CABI.CrossRefGoogle Scholar
  14. Ho, H. H., & Jong, S. C. (1991). Species concepts of Phytophthora cryptogea and P. drechsleri. Mycotaxon, 40, 35–39.Google Scholar
  15. Jeffers, S. N. (2006). Identifying species of Phytophthora. Clemson: Department of Entomology, Clemson University.Google Scholar
  16. Jönsson, U., Lundberg, L., Sonesson, K., & Jung, T. (2003). First records of soilborne Phytophthora species in Swedish oak forests. Forest Pathology, 33(3), 175–179.CrossRefGoogle Scholar
  17. Judelson, H. S., & Blanco, F. A. (2005). The spores of Phytophthora: Weapons of the plant destroyer. Nature Reviews Microbiology, 3(1), 47–58. Scholar
  18. Jung, T., & Blaschke, M. (2004). Phytophthora root and collar rot of alders in Bavaria: Distribution, modes of spread and possible management strategies. Plant Pathology, 53(2), 197–208.CrossRefGoogle Scholar
  19. Jung, T., & Burgess, T. I. (2009). Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp nov. Persoonia, 22, 95–110.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jung, T., Chang, T., Bakonyi, J., Seress, D., Pérez-Sierra, A., Yang, X., et al. (2017). Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology, 66(2), 194–211.CrossRefGoogle Scholar
  21. Jung, T., Orlikowski, L., Henricot, B., Abad-Campos, P., Aday, A. G., Aguin Casal, O., et al. (2016). Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46(2), 134–163.CrossRefGoogle Scholar
  22. Jung, T., Stukely, M. J. C., Hardy, G. S. J., White, D., Paap, T., Dunstan, W. A., et al. (2011). Multiple new Phytophthora species from ITS clade 6 associated with natural ecosystems in Australia: Evolutionary and ecological implications. Persoonia: Molecular Phylogeny and Evolution of Fungi, 26, 13–39.CrossRefGoogle Scholar
  23. Jungqvist, G., Oni, S. K., Teutschbein, C., & Futter, M. N. (2014). Effect of climate change on soil temperature in Swedish boreal forests. PLoS One, 9(4), e93957.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Larsson, M., & Gerhardson, B. (1990). Isolates of Phytophthora cryptogea pathogenic to wheat and some other crop plants. Journal of Phytopathology, 129(4), 303–315.CrossRefGoogle Scholar
  26. Larsson, M., & Gerhardson, B. (1992). Disease progression and yield losses from root diseases caused by soilborne pathogens of spinach. Phytopathology, 82(4), 403–406.CrossRefGoogle Scholar
  27. McKeever, K. M., & Chastagner, G. A. (2016). A survey of Phytophthora spp. associated with Abies in US Christmas tree farms. Plant Disease, 100(6), 1161–1169.CrossRefGoogle Scholar
  28. McKeever, K. M., & Chastagner, G. (2018). Interactions between root rotting Phytophthora, Abies christmas trees, and environment. Plant Disease.
  29. Nechwatal, J., Bakonyi, J., Cacciola, S. O., Cooke, D. E. L., Jung, T., Nagy, Z. A., Vannini, A., Vettraino, A. M., & Brasier, C. M. (2013). The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathology, 62(2), 355–369.CrossRefGoogle Scholar
  30. Nowak, K. J., Trzewik, A., Tulacz, D., Orlikowska, T., & Orlikowski, L. B. (2015). Characterization of polish Phytophthora lacustris isolates obtained from water environments. Polish Journal of Environmental Studies, 24(2), 619–630.Google Scholar
  31. Pettersson, M., Frampton, J., Ronnberg, J., Shew, H. D., Benson, D. M., Kohlway, W. H., et al. (2017a). Increased diversity of Phytophthora species in Fraser fir Christmas tree plantations in the southern Appalachians. Scandinavian Journal of Forest Research, 32(5), 412–420.CrossRefGoogle Scholar
  32. Pettersson, M., Frampton, J., & Sidebottom, J. (2017b). Influence of Phytophthora root rot on planting trends of Fraser fir Christmas trees in the southern Appalachian Mountains. Tree Planters' Notes, 60(1), 4–11.Google Scholar
  33. Quesada-Ocampo, L. M., Fulbright, D. W., & Hausbeck, M. K. (2009). Susceptibility of Fraser fir to Phytophthora capsici. Plant Disease, 93(2), 135–141.CrossRefGoogle Scholar
  34. Redondo, M. A., Boberg, J., Olsson, C. H. B., & Oliva, J. (2015). Winter conditions correlate with Phytophthora alni subspecies distribution in southern Sweden. Phytopathology, 105(9), 1191–1197.CrossRefPubMedGoogle Scholar
  35. Ristaino, J. B., Ivors, K., Bonans, P., Gómez-Alpizar, L., & Blanco-Meneses, M. (2010). Rapid diagnostic tools for Phytophthora on horticultural crops. Workshop: Implementación de herramientas de diagnóstico rápido para Phytophthora en cultivos agrícolas en Centro América. Universidad de Costa Rica, San José, Costa Rica Junio.Google Scholar
  36. Robideau, G. P., de Cock, A., Coffey, M. D., Voglmayr, H., Brouwer, H., Bala, K., et al. (2011). DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources, 11(6), 1002–1011.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Roos, J., Hopkins, R., Kvarnheden, A., & Dixelius, C. (2011). The impact of global warming on plant diseases and insect vectors in Sweden. European Journal of Plant Pathology, 129(1), 9–19.CrossRefGoogle Scholar
  38. Rytkonen, A., Lilja, A., Werres, S., Sirkia, S., & Hantula, J. (2013). Infectivity, survival and pathology of Finnish strains of Phytophthora plurivora and Ph. pini in Norway spruce. Scandinavian Journal of Forest Research, 28(4), 307–318.CrossRefGoogle Scholar
  39. Scanu, B., Linaldeddu, B. T., Deidda, A., & Jung, T. (2015). Diversity of Phytophthora species from declining Mediterranean maquis vegetation, including two new species, Phytophthora crassamura and P. ornamentata sp. nov. PLoS One, 10(12), e0143234.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shafizadeh, S., & Kavanagh, J. A. (2005). Pathogenicity of Phytophthora species and Pythium undulatum isolated from Abies procera Christmas trees in Ireland. Forest Pathology, 35(6), 444–450.CrossRefGoogle Scholar
  41. Talgø, V., & Chastagner, G. A. (2013). Phytophthora on Abies spp. (true firs). JKI Data Sheets-Plant Diseases and Diagnosis, 3.Google Scholar
  42. Talgø, V., Herrero, M., Toppe, B., Klemsdal, S., & Stensvand, A. (2006). First report of root rot and stem canker caused by Phytophthora cambivora on noble fir (Abies procera) for bough production in Norway. Plant Disease, 90(5), 682–682.CrossRefGoogle Scholar
  43. Talgø, V., Herrero, M. L., Toppe, B., Klemsdal, S. S., & Stensvand, A. (2007). Phytophthora root rot and stem canker found on Nordmann and subalpine fir in Norwegian Christmas tree plantations. Plant Health Progress.
  44. Talgø, V., Schmitz, S., Chandelier, A., Brurberg, M. B., & Thomsen, I. M. (2015). Baiting for Phytophthora in waterways associated with Christmas tree production in Norway, Belgium and Denmark. NIBIO BOOK, 1(1), 63.Google Scholar
  45. Talgø, V., Schmitz, S., Chandelier, A., Brurberg, M. B., & Thomsen, I. M. (2017). Baiting for Phytophthora in waterways associated with Christmas tree production in Norway, Belgium and Denmark. NIBIO BOOK, 3(6), 80–82.Google Scholar
  46. Telfer, K. H., Brurberg, M. B., Herrero, M. L., Stensvand, A., & Talgo, V. (2015). Phytophthora cambivora found on beech in Norway. Forest Pathology, 45(5), 415–425.CrossRefGoogle Scholar
  47. Werres, S., Wagner, S., Brand, T., Kaminski, K., & Seipp, D. (2007). Survival of Phytophthora ramorum in recirculating irrigation water and subsequent infection of Rhododendron and Viburnum. Plant Disease, 91(8), 1034–1044.CrossRefGoogle Scholar
  48. White, T. J., Bruns, T., Lee, S. J. W. T., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18(1), 315–322.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Martin Pettersson
    • 1
    Email author
  • John Frampton
    • 2
  • Jonas Rönnberg
    • 1
  • May Bente Brurberg
    • 3
    • 4
  • Venche Talgø
    • 3
  1. 1.Southern Swedish Forest Research CentreSwedish University of Agricultural SciencesAlnarpSweden
  2. 2.Department of Forestry and Environmental ResourcesNorth Carolina State UniversityRaleighUSA
  3. 3.Norwegian Institute of Bioeconomy ResearchÅsNorway
  4. 4.Norwegian University of Life ScienceÅsNorway

Personalised recommendations