Biological Invasions

, Volume 20, Issue 9, pp 2313–2328 | Cite as

Changes in the population structure and sporulation behaviour of Phytophthora ramorum associated with the epidemic on Larix (larch) in Britain

  • A. R. Harris
  • M. S. Mullett
  • J. F. Webber
Original Paper


During a decade of invasion, the exotic pathogen Phytophthora ramorum has undergone an unexpected change in behaviour during spread into the woodlands and forests of Great Britain. From 2002 to 2008 most outbreaks centred on nurseries and managed gardens with affected hosts almost exclusively broadleaf shrubs and trees. However 2009 saw a major shift as larch tree plantations (Larix) were affected by widespread infection and mortality incited by P. ramorum. To understand the processes underlying the host jump to larch, isolates of the EU1 lineage of P. ramorum collected from 2002 to 2012 were investigated using seven polymorphic microsatellite markers. Analysis of 347 isolates resolved 51 multilocus genotypes (MLGs) which partitioned into two distinct clusters. One comprised MLGs unique to Britain and unknown elsewhere in Europe, the other cluster was primarily of MLGs already known in other European countries but dominated by one genotype, EU1MG1. Pre-2009 isolates were predominantly of the unique British cluster with only a few typical of the European cluster. This reversed after 2009 with European MLGs, especially EU1MG1, becoming increasingly common as the larch epidemic expanded. We hypothesise that the growing dominance of EU1MLG1 has been an important driver in the emergence of the epidemic on larch, aided by its ability to sporulate more abundantly compared with the dominant unique British MLG. European MLGs appear closely associated with the distribution of larch along the west coast of Britain whereas unique British MLGs tend to be concentrated in south west England. The two population clusters suggest at least two separate introductions of the EU1 lineage into Britain with subsequent diversification.


Genetic diversity Sudden larch death EU1 lineage Microsatellites Invasive 



We thank the Forestry Commission and Imperial College London for funding and supporting this research. Thanks also to Kris Van Poucke (Institute for Agriculture, Fisheries and Food (ILVO), Belgium) for invaluable advice on allele scoring and MLG nomenclature. Finally, we are grateful to Forest Research Statistician Jack Forster for statistical advice on the analysis of the sporulation data and also to many Forest Research colleagues who over several years have contributed to the Phytophthora Culture Collection which formed the basis of this study.

Supplementary material

10530_2018_1702_MOESM1_ESM.docx (47 kb)
Supplementary material 1 (DOCX 47 kb)


  1. Anon (2008) Phytophthora ramorum a practical guide for established parks and gardens, amenity landscape and woodland trees. Accessed 13 April 2018
  2. Boutet X, Vercauteren A, Heungens K, Laurent F, Chandelier A (2010) Oospore progenies from Phytophthora ramorum. Fungal Biol 114:369–378CrossRefGoogle Scholar
  3. Brasier CM, Webber JF (2010) Sudden larch death. Nature 466:824–825CrossRefPubMedGoogle Scholar
  4. Brasier CM, Kirk SA, Webber JF (2007) Report on the probability of sexual recombination between European A1 and American A2 isolates. Forest Research, Farnham, UK. Deliverable Report 11. EU Sixth Framework Project, RAPRAGoogle Scholar
  5. Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106CrossRefPubMedGoogle Scholar
  6. Chadfield V, Pautasso M (2012) Phytophthora ramorum in England and Wales: which environmental variables predict country disease incidence? For Pathol 42:150–159CrossRefGoogle Scholar
  7. Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Comput Syst 1695:1–9Google Scholar
  8. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  9. DSF (Département de la Santé des Forêts) (2017) La Lettre du DSF. No 51. Accessed 5 June 2017
  10. FERA (2012) Development of expertise in analysis of genetic diversity of Phytophthora ramorum using microsatellite markers. Report number: RB539007Google Scholar
  11. Goodwin SB (1997) The population genetics of Phytophthora. Phytopathology 87:462–473CrossRefPubMedGoogle Scholar
  12. Goss EM, Larsen M, Chastagner GA, Givens DR, Grünwald NJ (2009) Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Pathog 5:e1000583. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746CrossRefPubMedGoogle Scholar
  14. Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20:131–138CrossRefPubMedGoogle Scholar
  15. Grünwald NJ, Larsen MM, Kamvar ZN (2016) First report of the EU1 clonal lineage of Phytophthora ramorum on tanoak in an Oregon forest. Plant Dis 100:1054CrossRefGoogle Scholar
  16. Hansen EM, Kanaskie A, Prospero S, McWilliams M, Goheen EM, Osterbauer N, Reeser P, Sutton W (2008) Epidemiology of Phytophthora ramorum in Oregon tanoak forests. Can J For Res 38:1133–1143CrossRefGoogle Scholar
  17. Harris AR, Webber JF (2016) Sporulation potential, symptom expression and detection of Phytophthora ramorum on larch needles and other foliar hosts. Plant Pathol 65:1441–1451CrossRefGoogle Scholar
  18. Ivors K, Garbelotto M, Vries IDE, Ruyter-Spira C, Hekkert BTE, Rosenzweig N, Bonants P (2006) Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Mol Ecol 15:1493–1505CrossRefPubMedGoogle Scholar
  19. Kamoun S, Furzer O, Jones JDG, Judelson HS, Ali G, Dali RJD, Roy SG, Schena L, Zambounis A, Panabières F, Cahill D, Ruocco M, Figueiredo A, Chen X-R, Hulvey J, Stam R, Lamour K, Gijzen M, Tyler BM, Grünwald NJ, Mukhtar MS, Tomé DFA, Tör M, VanDen Ackerveken G, McDowell J, Daayf F, Fry WE, Lindqvist-Kreuze H, Meijer HJG, Petre B, Ristaino J, Yoshida K, Birch PRJ, Govers F (2015) The top 10 oomycete pathogens in molecular plant pathology. Mol Plant Pathol 16:413–434CrossRefPubMedGoogle Scholar
  20. Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. Peer J 2:e281CrossRefPubMedGoogle Scholar
  21. King K, Harris AR, Webber JF (2015) In planta detection used to define the distribution of the European lineages of Phytophthora ramorum on larch (Larix) in the UK. Plant Pathol 64:1168–1175CrossRefGoogle Scholar
  22. Mascheretti S, Croucher PJP, Vettraino A, Prospero S, Garbelotto M (2008) Reconstruction of the sudden oak death epidemic in California through microsatellite markers in Phytophthora ramorum. Mol Ecol 17:2755–2768CrossRefPubMedGoogle Scholar
  23. Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846CrossRefPubMedGoogle Scholar
  24. Nei M (1978) Estimation of average heterozygosities and genetic distance from a small numbers of individuals. Genetics 89:583–590PubMedPubMedCentralGoogle Scholar
  25. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: Community ecology package. R package version 2.0-7. Online publication.
  26. Peakal R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  27. Pérez-Sierra A, Álvarez LA, Vercauteren A, Heungens K, Abad-Campos P (2011) Genetic diversity, sensitivity to phenylamide fungicides and aggressiveness of Phytophthora ramorum on Camellia, Rhododendron and Viburnum plants in Spain. Plant Pathol 60:1069–1076CrossRefGoogle Scholar
  28. Prospero S, Hansen EM, Grünwald NJ, Winton LM (2007) Population dynamics of the sudden oak death pathogen Phytophthora ramorum in Oregon from 2001 to 2004. Mol Ecol 16:2958–2973CrossRefPubMedGoogle Scholar
  29. Prospero S, Vercauteren A, Heungens K, Belbahri L, Rigling D (2013) Phytophthora diversity and population structure of Phytophthora ramorum in Swiss ornamental nurseries. Plant Pathol 62:1063–1071CrossRefGoogle Scholar
  30. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  31. Rizzo DM, Garbelotto M, Hansen EM (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–335CrossRefPubMedGoogle Scholar
  32. Sansford CE, Inman AJ, Baker R, Brasier CM, Frankel S, de Gruyter J, Husson C, Kehlenbeck H, Kessell G, Moralejo E, Steeghs M, Webber J, Werres S (2009) Risk analysis for Phytophthora ramorum, a newly recognised pathogen threat to Europe and the cause of Sudden Oak Death in the USA (RAPRA). EU 6th Framework Project RAPRA, Deliverable Report 28 Accessed 13 April 2018
  33. Schlenzig A, Cooke D (2012) Genetic diversity of Phytophthora ramorum in nursery trade and managed environment in Scotland. In: Frankel SJ, Palmieri KM, Alexander J (eds) General Technical Report PSW-GTR-243. Proceedings of the fifth sudden oak death science symposium, 19–22 June 2012, Petaluma, CA. USDA Forest Service, Albany, pp 33–39Google Scholar
  34. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  35. Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711PubMedPubMedCentralGoogle Scholar
  36. Tracy DR (2009) Phytophthora ramorum and Phytophthora kernoviae: the woodland perspective. EPPO Bull 39:161–167CrossRefGoogle Scholar
  37. Van Poucke K, Vercauteren A, Maes M, Werres S Heungens K (2012a) Genotypic diversity of European Phytophthora ramorum isolates based on SSR analysis. In: Frankel SJ, Kliejunas JT, Palmieri KM, Alexander JM (eds) General technical report PSW-GTR-243. Proceedings of the fifth sudden oak death science symposium, 19–22 June 2012, Petaluma, CA. USDA Forest Service, Albany, p 40Google Scholar
  38. Van Poucke K, Franceschini S, Webber JF, Vercauteren A, Turner J, McCracken AR, Heungens K, Brasier CM (2012b) Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biol 116:1178–1191CrossRefPubMedGoogle Scholar
  39. Vercauteren A, De Dobbelaere I, Grünwald NJ, Bonants PJM, Van Bockstaele E, Maes M, Heungens K (2010) Clonal expansion of the Belgium Phytophthora ramorum populations based on new microsatellite markers. Mol Ecol 19:92–107CrossRefPubMedGoogle Scholar
  40. Vercauteren A, De Dobbelaere I, Van Bockstaele E, Maes M, Heungens K (2011) Genotypic and phenotypic characterization of the European A2 isolates of Phytophthora ramorum. Eur J Plant Pathol 129:621–635CrossRefGoogle Scholar
  41. Webber JF, Brasier CM (2018) Ramorum disease of larch. In: Hansen EM, Lewis KJ (eds) Compendium of conifer diseases and pests in forests and christmas tree. The American Phytopathological Society, St. PaulGoogle Scholar
  42. Webber JF, Mullett M, Brasier CM (2010) Dieback and mortality of plantation Japanese larch (Larix kaempferi) associated with infection by Phytophthora ramorum. New Dis Rep 22:19CrossRefGoogle Scholar
  43. Werres S, Marwitz R, Man In’t Veld WA, De Cock AWAM, Bonants PJM, De Weerdt M, Themann K, Ilieva E, Baayen RP (2001) Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycol Res 105:1155–1165CrossRefGoogle Scholar

Copyright information

© Crown 2018

Authors and Affiliations

  • A. R. Harris
    • 1
    • 2
  • M. S. Mullett
    • 1
    • 2
  • J. F. Webber
    • 2
  1. 1.Division of Biology, Department of Life SciencesImperial College LondonAscotUK
  2. 2.Forest ResearchFarnhamUK

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