1932

Abstract

The sudden oak and sudden larch death pathogen emerged simultaneously in the United States on oak and in Europe on in the 1990s. This pathogen has had a devastating impact on larch plantations in the United Kingdom as well as mixed conifer and oak forests in the Western United States. Since the discovery of this pathogen, a large body of research has provided novel insights into the emergence, epidemiology, and genetics of this pandemic. Genetic and genomic resources developed for have been instrumental in improving our understanding of the epidemiology, evolution, and ecology of this disease. The recent reemergence of EU1 in the United States and EU2 in Europe and the discovery of in Asia provide renewed impetus for research on the sudden oak death pathogen.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-082718-100117
2019-08-25
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/phyto/57/1/annurev-phyto-082718-100117.html?itemId=/content/journals/10.1146/annurev-phyto-082718-100117&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Anagnostakis SL. 1987. Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:123–37
    [Google Scholar]
  2. 2. 
    Bollmann SR, Press CM, Tyler BM, Grünwald NJ 2018. Expansion and divergence of Argonaute genes in the oomycete genus Phytophthora. Front. Microbiol 9:2841
    [Google Scholar]
  3. 3. 
    Boutet X, Vercauteren A, Heungens K, Laurent F, Chandelier A 2010. Oospores progenies from Phytophthora ramorum. Fungal Biol 114:4369–78
    [Google Scholar]
  4. 4. 
    Brasier C. 1991. Ophiostoma novo-ulmi sp. nov., causative agent of current Dutch elm disease pandemics. Mycopathologia 115:3151–61
    [Google Scholar]
  5. 5. 
    Brasier C, Kirk S, Rose J 2006. Differences in phenotypic stability and adaptive variation between the main European and American lineages of Phytophthora ramorum. Progress in Research on Phytophthora Diseases of Forest Trees CM Brasier, T Jung, W Oßwald 166–73 Farnham, UK: For. Res.
    [Google Scholar]
  6. 6. 
    Brasier C, Kirk S, Webber J 2007. Report on the probability of sexual recombination between European A1 and American A2 isolates UK Deliv. Rep. 11, For. Res Farnham, UK:
  7. 7. 
    Brasier C, Webber J. 2010. Sudden larch death: plant pathology. Nature 466:7308824–25
    [Google Scholar]
  8. 8. 
    Brasier CM, Vettraino AM, Chang TT, Vannini A 2010. Phytophthora lateralis discovered in an old growth Chamaecyparis forest in Taiwan. Plant Pathol 59:4595–603
    [Google Scholar]
  9. 9. 
    Cobb RC, Rizzo DM. 2016. Litter chemistry, community shift, and non-additive effects drive litter decomposition changes following invasion by a generalist pathogen. Ecosystems 19:81478–90
    [Google Scholar]
  10. 10. 
    Croucher PJP, Mascheretti S, Garbelotto M 2013. Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California. Biol. Invasions 15:102281–97
    [Google Scholar]
  11. 11. 
    Cunniffe NJ, Cobb RC, Meentemeyer RK, Rizzo DM, Gilligan CA 2016. Modeling when, where, and how to manage a forest epidemic, motivated by sudden oak death in California. PNAS 113:205640–45Used mathematical modeling to explore control options for invasive plant pathogens in complex spatiotemporal landscapes.
    [Google Scholar]
  12. 12. 
    Dale AL. 2018. Using genomic data to understand anthropogenic influences on oomycete andPhytophthoracommunities, and the evolution of an alien invasive species responsible for sudden oak death, Phytophthora ramorum PhD Thesis, Univ. B. C Vancouver:
    [Google Scholar]
  13. 13. 
    Dale AL, Feau N, Everhart SE, Dhillon B, Wong B et al. 2019. Mitotic recombination and a two-speed genome shape the evolution of asexual lineages of the sudden oak death pathogen Phytophthora ramorum. mBio 10:2e02452–18Largest genome resequencing study of P. ramorum, covering all four known lineages.
    [Google Scholar]
  14. 14. 
    Donahoo R, Blomquist CL, Thomas SL, Moulton JK, Cooke DEL, Lamour KH 2006. Phytophthora foliorum sp. nov., a new species causing leaf blight of azalea. Mycol. Res. 110:111309–22
    [Google Scholar]
  15. 15. 
    Dong S, Raffaele S, Kamoun S 2015. The two-speed genomes of filamentous pathogens: waltz with plants. Curr. Opin. Genet. Dev. 35:57–65
    [Google Scholar]
  16. 16. 
    Elliott M, Sumampong G, Varga A, Shamoun S, James D et al. 2011. Phenotypic differences among three clonal lineages of Phytophthora ramorum. For. Pathol 41:17–14
    [Google Scholar]
  17. 17. 
    Elliott M, Yuzon J, C MM, Tripathy S, Bui M et al. 2018. Characterization of phenotypic variation and genome aberrations observed among Phytophthora ramorum isolates from diverse hosts. BMC Genom 19:1320
    [Google Scholar]
  18. 18. 
    Everhart SE, Tabima JF, Grünwald NJ 2014. Phytophthora ramorum. Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens RA Dean, A Lichens-Park, C Kole 159–74 Berlin: Springer
    [Google Scholar]
  19. 19. 
    Fahlgren N, Bollmann SR, Kasschau KD, Cuperus JT, Press CM et al. 2013. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLOS ONE 8:10e77181
    [Google Scholar]
  20. 20. 
    Feau N, Taylor G, Dale AL, Dhillon B, Bilodeau GJ et al. 2016. Genome sequences of six Phytophthora species threatening forest ecosystems. Genom. Data 10:85–88
    [Google Scholar]
  21. 21. 
    Fichtner EJ, Lynch SC, Rizzo DM 2007. Detection, distribution, sporulation, and survival of Phytophthora ramorum in a California redwood-tanoak forest soil. Phytopathology 97:101366–75
    [Google Scholar]
  22. 22. 
    Flier WG, Grünwald NJ, Fry WE, Turkensteen LJ 2001. Formation, production and viability of oospores of Phytophthora infestans from potato and Solanum demissum in the Toluca Valley, central Mexico. Mycol. Res. 105:998–1006
    [Google Scholar]
  23. 23. 
    Flier WG, Grünwald NJ, Kroon L, Sturbaum AK, van den Bosch TBM et al. 2003. The population structure of Phytophthora infestans from the Toluca Valley of central Mexico suggests genetic differentiation between populations from cultivated potato and wild Solanum spp. Phytopathology 93:4382–90
    [Google Scholar]
  24. 24. 
    Forche A, Abbey D, Pisithkul T, Weinzierl MA, Ringstrom T et al. 2011. Stress alters rates and types of loss of heterozygosity in Candida albicans. mBio 2:4e00129–11
    [Google Scholar]
  25. 25. 
    Frankel SJ. 2008. Sudden oak death and Phytophthora ramorum in the USA: a management challenge. Australas. Plant Pathol. 37:119–25
    [Google Scholar]
  26. 26. 
    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 5:9e1000583
    [Google Scholar]
  27. 27. 
    Goss EM, Larsen M, Vercauteren A, Werres S, Heungens K, Grünwald NJ 2011. Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology 101:1166–71
    [Google Scholar]
  28. 28. 
    Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE et al. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. PNAS 111:248791–96
    [Google Scholar]
  29. 29. 
    Griesbach JA, Parke JL, Chastagner GA, Grünwald NJ, Aguirre J 2012. Safe Procurement and Production Manual Wisonville, OR: Or. Assoc. Nurs.
  30. 30. 
    Grünwald NJ, Flier WG. 2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171–90
    [Google Scholar]
  31. 31. 
    Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S 2012. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20:3131–38
    [Google Scholar]
  32. 32. 
    Grünwald NJ, Garbelotto M, Martin FN, Prospero S, Hansen E et al. 2009. Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology 99:7792–95Describes standards for naming clonal linages of the sudden oak death pathogen Phytophthora ramorum.
    [Google Scholar]
  33. 33. 
    Grünwald NJ, Goss EM, Press CM 2008. Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Mol. Plant Pathol. 9:6729–40
    [Google Scholar]
  34. 34. 
    Grünwald NJ, Larsen MM, Kamvar ZN, Reeser PW, Kanaskie A et al. 2016. First report of the EU1 clonal lineage of Phytophthora ramorum on tanoak in an Oregon forest. Plant Dis 100:51024
    [Google Scholar]
  35. 35. 
    Grünwald NJ, Werres S, Goss EM, Taylor CR, Fieland VJ 2012. Phytophthora obscura sp. nov., a new species of the novel Phytophthora subclade 8. Plant Pathol 61:3610–22
    [Google Scholar]
  36. 36. 
    Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:7262393–98
    [Google Scholar]
  37. 37. 
    Hansen EM, Goheen DJ, Jules ES, Ullian B 2000. Managing Port-Orford-cedar and the introduced pathogen Phytophthora lateralis. Plant Dis 84:14–14
    [Google Scholar]
  38. 38. 
    Hansen EM, Kanaskie A, Prospero S, McWilliams M, Goheen EM et al. 2008. Epidemiology of Phytophthora ramorum in Oregon tanoak forests. Can. J. For. Res. 38:51133–43
    [Google Scholar]
  39. 39. 
    Hansen EM, Streito J, Delatour C 1999. First confirmation of Phytophthora lateralis in Europe. Plant Dis 83:6587
    [Google Scholar]
  40. 40. 
    Harris AR, Mullett MS, Webber JF 2018. Changes in the population structure and sporulation behaviour of Phytophthora ramorum associated with the epidemic on Larix (larch) in Britain. Biol. Invasions 20:92313–28
    [Google Scholar]
  41. 41. 
    Harris AR, Webber JF. 2016. Sporulation potential, symptom expression and detection of Phytophthora ramorum on larch needles and other foliar hosts. Plant Pathol 65:91441–51
    [Google Scholar]
  42. 42. 
    Harvell CD. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296:55762158–62
    [Google Scholar]
  43. 43. 
    Hayden KJ, Garbelotto M, Knaus BJ, Cronn RC, Rai H, Wright JW 2014. Dual RNA-seq of the plant pathogen Phytophthora ramorum and its tanoak host. Tree Genet. Genomes 10:3489–502
    [Google Scholar]
  44. 44. 
    Ivors K, Garbelotto M, Vries IDE, Ruyter-Spira C, Hekkert BT et al. 2006. Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Mol. Ecol. 15:61493–505
    [Google Scholar]
  45. 45. 
    Jiang RHY, Tripathy S, Govers F, Tyler BM 2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. PNAS 105:124874–79
    [Google Scholar]
  46. 46. 
    Jung T, Pérez-Sierra A, Rees H, Scanu B, Bakonyi J et al. 2017. Diversity of Phytophthora species in natural forests and streams and in rubber plantations in Vietnam. Proceedings of the 8th Meeting of the International Union of Forestry Research Organizations, Phytophthora in Forests and Natural Ecosystems56 Vienna, Austria: IUFRO https://www.iufro.org/fileadmin/material/publications/proceedings-archive/70209-vietnam17-abstracts.pdf
    [Google Scholar]
  47. 47. 
    Kamvar ZN, Larsen MM, Kanaskie AM, Hansen EM, Grünwald NJ 2015. Spatial and temporal analysis of populations of the sudden oak death pathogen in Oregon forests. Phytopathology 105:7982–89
    [Google Scholar]
  48. 48. 
    Kasuga T, Bui M, Bernhardt E, Swiecki T, Aram K et al. 2016. Host-induced aneuploidy and phenotypic diversification in the sudden oak death pathogen Phytophthora ramorum. BMC Genom 17:1385
    [Google Scholar]
  49. 49. 
    Kasuga T, Kozanitas M, Bui M, Hüberli D, Rizzo DM, Garbelotto M 2012. Phenotypic diversification is associated with host-induced transposon derepression in the sudden oak death pathogen Phytophthora ramorum. PLOS ONE 7:4e34728
    [Google Scholar]
  50. 50. 
    King KM, 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 64:51168–75
    [Google Scholar]
  51. 51. 
    Kinloch BB. 2003. White pine blister rust in North America: past and prognosis. Phytopathology 93:81044–47
    [Google Scholar]
  52. 52. 
    Kovacs K, Václavík T, Haight RG, Pang A, Cunniffe NJ et al. 2011. Predicting the economic costs and property value losses attributed to sudden oak death damage in California (2010–2020). J. Environ. Manag. 92:41292–302
    [Google Scholar]
  53. 53. 
    LeBoldus JM, Sondreli K, Sutton W, Reeser PW, Kanaskie A et al. 2017. First report of Phytophthora ramorum lineage EU1 infecting Douglas fir and grand fir in Oregon. Plant Dis 102:2455
    [Google Scholar]
  54. 54. 
    Mascheretti S, Croucher PJP, Vettraino A, Prospero S, Garbelotto M 2008. Reconstruction of the sudden oak death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum. Mol. Ecol 17:112755–68
    [Google Scholar]
  55. 55. 
    Morris PF, Phuntumart V. 2009. Inventory and comparative evolution of the ABC superfamily in the genomes of Phytophthora ramorum and Phytophthora sojae. J. Mol. Evol 68:5563–75
    [Google Scholar]
  56. 56. 
    Nelson H, Grace P, McBeath A, Stennes B 2009. Estimating the potential returns from developing a national forest pest strategy: the benefits of developing a proactive approach to managing risk Can. For. Serv. Rep., Pac. For. Cent Vancouver:
  57. 57. 
    Peterson E, Hansen E, Hulbert J 2014. Source or sink? The role of soil and water borne inoculum in the dispersal of Phytophthora ramorum in Oregon tanoak forests. For. Ecol. Manag. 322:48–57
    [Google Scholar]
  58. 58. 
    Peterson EK, Hansen EM, Kanaskie A 2015. Temporal epidemiology of sudden oak death in Oregon. Phytopathology 105:7937–46
    [Google Scholar]
  59. 59. 
    Pfister S. 2011. Phytophthora ramorum program past, present and future direction. Presented at the Annual Meeting of the National Plant Board, Denver, CO, Aug 7–11 https://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/PramorumNPB2011Pfister.pdf
  60. 60. 
    Prospero S, Grünwald NJ, Winton LM, Hansen EM 2009. Migration patterns of the emerging plant pathogen Phytophthora ramorum on the West Coast of the United States of America. Phytopathology 99:6739–49
    [Google Scholar]
  61. 61. 
    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. 16:142958–73
    [Google Scholar]
  62. 62. 
    Rizzo DM, Garbelotto M. 2003. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1:4197–204
    [Google Scholar]
  63. 63. 
    Rizzo DM, Garbelotto M, Davidson JM, Slaughter GW, Koike ST 2002. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis 86:3205–14
    [Google Scholar]
  64. 64. 
    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. 43:1309–35
    [Google Scholar]
  65. 65. 
    Sambles C, Schlenzig A, O'Neill P, Grant M, Studholme DJ 2015. Draft genome sequences of Phytophthora kernoviae and Phytophthora ramorum lineage EU2 from Scotland. Genom. Data 6:193–94
    [Google Scholar]
  66. 66. 
    Schenck N, Saurat C, Guinet C, Fourrier-Jeandel C, Roche L et al. 2018. First report of Phytophthora ramorum causing Japanese larch dieback in France. Plant Dis 102:222045
    [Google Scholar]
  67. 67. 
    Schlenzig A, Purser E, Perez-Sierra A 2016. First finding of Phytophthora foliorum in the United Kingdom. New Dis. Rep. 34:2
    [Google Scholar]
  68. 68. 
    Shamoun SF, Rioux D, Callan B, James D, Hamelin RC et al. 2018. An overview of Canadian research activities on diseases caused by Phytophthora ramorum: results, progress, and challenges. Plant Dis 102:71218–33
    [Google Scholar]
  69. 69. 
    Tomlinson I. 2016. The discovery of ash dieback in the UK: the making of a focusing event. Environ. Politics 25:4709–28
    [Google Scholar]
  70. 70. 
    Turner J, O'Neill P, Grant M, Mumford RA, Thwaites R, Studholme DJ 2017. Genome sequences of 12 isolates of the EU1 lineage of Phytophthora ramorum, a fungus-like pathogen that causes extensive damage and mortality to a wide range of trees and other plants. Genom. Data 12:17–21
    [Google Scholar]
  71. 71. 
    Tyler BM, Putnam NH, Phuntumart V, Morris PF, Sakihama Y et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:57911261–66The first two oomycete genomes sequenced including Phytophthora ramorum and P. sojae describing RxLR discovery.
    [Google Scholar]
  72. 72. 
    Univ. Calif. Div. Agric. Nat. Resour 2019. Best management practices by applicable pests: Phytophthora ramorum (P.r). University of California, Division of Agriculture and Natural Resources http://ucnfa.ucanr.edu/Grants_and_Projects/CANGC_Unified_BMPs_Project/Pests/?ds=630&reportnumber=1172&catcol=4283&categorysearch=Phytophthora%20ramorum%20%28P%2Er%29
    [Google Scholar]
  73. 73. 
    USDA-APHIS 2011. Re-assessing Phytophthora ramorum regulatory framework: impact of pathogen presence in commercial nurseries and wild land environments Exec. Summ., USDA-APHIS Riverdale, MD: https://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/PramFrameworkConceptPaper.pdf
    [Google Scholar]
  74. 74. 
    Van Poucke K, Franceschini S, Webber JF, Vercauteren A, Turner JA et al. 2012. Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biol 116:111178–91
    [Google Scholar]
  75. 75. 
    Vercauteren A, De Dobbelaere I, Grünwald NJ, Bonants P, Van Bockstaele E et al. 2010. Clonal expansion of the Belgian Phytophthora ramorum populations based on new microsatellite markers. Mol. Ecol. 19:192–107
    [Google Scholar]
  76. 76. 
    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 129:4621–35
    [Google Scholar]
  77. 77. 
    Webber J. 2017. Phytophthora ramorum: update on the impact and wider consequences of the epidemic in Britain. Proceedings of the Sixth Sudden Oak Death Science Symposium4–6 Albany, CA: USDA For. Serv.
    [Google Scholar]
  78. 78. 
    Werres S, Marwitz R, Veld W, De Cock A, Bonants PJM et al. 2001. Phytophthora ramorum sp nov., a new pathogen on Rhododendron and Viburnum. Mycol. Res 105:1155–65
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-082718-100117
Loading
/content/journals/10.1146/annurev-phyto-082718-100117
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error