Sudden oak death: Interactions of the exotic oomycete phytophthora ramorum with naïve North American hosts

Eukaryotic Cell

Volumn 11, Issue 11, 2012, Pages 1313-1323

  Garbelotto, Matteo ^a   Hayden, Katherine J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASSIFICATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOST PARASITE INTERACTION; NORTH AMERICA; OAK; PARASITOLOGY; PATHOGENICITY; PHYTOPHTHORA; PLANT DISEASE; PLANT LEAF; REVIEW; SEASON; SOIL; TEMPERATURE;

GENETIC VARIATION; GENOTYPE; HOST-PARASITE INTERACTIONS; NORTH AMERICA; PHYTOPHTHORA; PLANT DISEASES; PLANT LEAVES; QUERCUS; SEASONS; SOIL; TEMPERATURE;

PHYTOPHTHORA RAMORUM; QUERCUS;

EID: 84868143725     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00195-12     Document Type: Review

References (128)

1. Anacker B, et al. 2008. Susceptibility to Phytophthora ramorum in a key infectious host: landscape variation in host genotype, host phenotype, and environmental factors. New Phytol. 177:756-766.
2. Animal and Plant Health Inspection Service, United States Department of Agriculture. 2012. Domestic quarantine notices, subpart Phytophthora ramorum. Title 7 CFR §301.92.
3. Antia R, Regoes RR, Koella JC, Bergstrom CT. 2003. The role of evolution in the emergence of infectious diseases. Nature 426:658-661.
4. Bimpong EC, Clerk GC. 1970. Motility and chemotaxis in zoospores of Phytophthora palmivora. Ann. Bot. 34:716-724.
5. Boutet X, Vercauteren A, Heungens K, Laurent F, Chandelier A. 2010. Oospores progenies from Phytophthora ramorum. Fungal Biol. 114:369-378.
6. Brasier C, et al. 2004. Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol. Res. 108:1172-1184.
7. Brasier CM, Vettraino AM, Chang TT, Vannini A. 2010. Phytophthora lateralis discovered in an old growth Chamaecyparis forest in Taiwan. Plant Pathol. 59:595-603.
8. Brasier C. 2003. Sudden oak death: Phytophthora ramorum exhibits transatlantic differences. Mycol. Res. 107:258-259.
9. Brasier C, Denman S, Brown A, Webber J. 2004. Sudden oak death (Phytophthora ramorum) discovered on trees in Europe. Mycol. Res. 108: 1108-1110.
10. Brasier C, Kirk S. 2004. Production of gametangia by Phytophthora ramorum in vitro. Mycol. Res. 108:823-827.
11. Brasier C, Webber J. 2010. Plant pathology: sudden larch death. Nature 466:824-825.
12. Brown LB, Allen-Diaz B. 2009. Forest stand dynamics and sudden oak death: mortality in mixed-evergreen forests dominated by coast live oak. For. Ecol. Manage. 257:1271-1280.
13. Cherubini P, Dobbertin M, Innes JL. 1998. Potential sampling bias in long-term forest growth trends reconstructed from tree rings: a case study from the Italian Alps. For. Ecol. Manage. 109:103-118.
14. Chimento A, Cacciola SO, Garbelotto M. 2012. Detection of mRNA by reverse-transcription PCR as an indicator of viability in Phytophthora ramorum. For. Pathol. 42:14-21.
15. Cobb R, Lynch SC, Meentemeyer R, Rizzo DM. 2008. Five years of monitoring infection and mortality in redwood tanoak forests, p 215-218. In Frankel SJ, Kliejunas JT, Palmieri KM (ed), Proceedings of the sudden oak death third science symposium. USDA-Forest Service Pacific Southwest Research Station, Albany, CA.
16. Cobb R, Meentemeyer R, Rizzo D. 2010. Apparent competition in canopy trees determined by pathogen transmission rather than susceptibility. Ecology 91:327-333.
17. Cobb RC, Filipe JAN, Meentemeyer RK, Gilligan CA, Rizzo DM. 2012. Ecosystem transformation by emerging infectious disease: loss of large tanoak from California forests. J. Ecol. 712-722.
18. Cobb R, Chan M, Meentemeyer R, Rizzo D. 2012. Common factors drive disease and coarse woody debris dynamics in forests impacted by sudden oak death. Ecosystems 15:242-255.
19. Collins B, Parke J, Lachenbruch B, Hansen E. 2009. The effects of Phytophthora ramorum infection on hydraulic conductivity and tylosis formation in tanoak sapwood. Can. J. For. Res. 39:1766-1776.
20. COMTF. 2007. California Oak Mortality Task Force report, November 2007. University of California, Berkeley, Center for Forestry, Berkeley, CA. http://www.suddenoakdeath.org/.
21. Conrad A, Bonello P, Mcpherson BA, Wood D, Opiyo S, Mori S. Metabolite profiling to predict resistance to Phytophthora ramorum in natural populations of coast live oak. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
22. Croucher P, Mascheretti S, Garbelotto M. Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion genetics of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
23. Cushman J, Meentemeyer R. 2008. Multi-scale patterns of human activity and the incidence of an exotic forest pathogen. J. Ecol. 96:766-776.
24. Dart NL, Chastagner GA, Rugarber EF, Riley KL. 2007. Recovery frequency of Phytophthora ramorum and other Phytophthora spp. in the soil profile of ornamental retail nurseries. Plant Dis. 91:1419-1422.
25. Davidson JM, Wickland AC, Patterson HA, Falk KR, Rizzo DM. 2005. Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95:587-596.
26. Davidson JM, Patterson HA, Wickland AC, Fichtner EJ, Rizzo DM. 2011. Forest type influences transmission of Phytophthora ramorum in California oak woodlands. Phytopathology 101:492-501.
27. Davidson J, Patterson H, Rizzo D. 2008. Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology 98:860-866.
28. Davidson J, et al. 2004. Evidence for aerial transmission of Phytophthora ramorum among Quercus and Lithocarpus in California woodlands, p 108-114. In McComb JA, Hardy GE, Tommerup IC (ed), Phytophthora in forests and natural ecosystems. Proceedings of 2nd International IUFRO Working Party 7.02.09 Meeting, Albany, W. Australia. 20th Sept.-5th Oct. 2001. Murdoch University Print, Perth, Australia.
29. Davidson J, Werres S, Garbelotto M, Hansen E, Rizzo D. 2003. Sudden oak death and associated diseases caused by Phytophthora ramorum. PHP doi:10.1094/PHP-2003-0707-01-DG.
30. Davis F, Borchert M, Meentemeyer R, Flint A, Rizzo D. 2010. Preimpact forest composition and ongoing tree mortality associated with sudden oak death in the Big Sur region, California. For. Ecol. Manage. 259:2342-2354.
31. Dileo M, Bostock R, Rizzo D. 2009. Phytophthora ramorum does not cause physiologically significant systemic injury to California bay laurel, its primary reservoir host. Phytopathology 99:1307-1311.
32. Dodd R, et al. 2005. Is variation in susceptibility to Phytophthora ramorum correlated with population genetic structure in coast live oak (Quercus agrifolia)? New Phytol. 165:203-214.
33. Dodd R, et al. 2008. Evidence for the role of synchronicity between host phenology and pathogen activity in the distribution of sudden oak death canker disease. New Phytol. 179:505-514.
34. Dybiec B, Kleczkowski A, Gilligan CA. 2009. Modelling control of epidemics spreading by long-range interactions. J. R. Soc. Interface 6:941-950.
35. EFSA Panel on Plant Health. 2011. Scientific opinion on the pest risk analysis on Phytophthora ramorum prepared by the FP6 project RAPRA. EFSA J. 9:2186-2292. doi:10.2903/j.efsa.2011.2186.
36. Elliott M, et al. 2011. Phenotypic differences among three clonal lineages of Phytophthora ramorum. For. Pathol. 41:7-14.
37. Englander L, Tooley P. 2003. Plant hosts in the nursery industry-PLANTS MOVE! How might the movement of plants in the nursery industry contribute to the spread of Phytophthora ramorum to new areas? Sudden Oak Death Online Symposium. www.scientificsocieties.org/aps /proceedings/sod/pdf/englander.pdf.
38. Erwin DC, Ribeiro OK. 1996. Phytophthora diseases worldwide. APS Press, St. Paul, MN.
39. Eyre C, Kozanitas M, Garbelotto M. Population dynamics of aerial and terrestrial populations of Phytophthora ramorum in a California watershed under different climatic conditions. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
40. Fichtner E, Lynch S, Rizzo D. 2009. Survival, dispersal, and potential soil-mediated suppression of Phytophthora ramorum in a California redwood-tanoak forest. Phytopathology 99:608-619.
41. Fichtner EJ, Lynch SC, Rizzo DM. 2007. Detection, distribution, sporulation, and survival of Phytophthora ramorum in a California redwoodtanoak forest soil. Phytopathology 97:1366-1375.
42. Fry WE, Goodwin SB. 1997. Re-emergence of potato and tomato late blight in the United States. Plant Dis. 81:1349-1357.
43. Garbelotto M, et al. 2002. Non-oak native plants are main hosts for sudden oak death pathogen in California. Calif. Agric. 57:18-23.
44. Garbelotto M, Hayden K, Swain S, Schmidt D. Long-term monitoring of P. ramorum inoculum identifies spatio-temporal patterns of pathogen sporulation and proves that selective bay removal reduces risk of oak infection. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
45. Garbelotto M, Rizzo D. 2005. A California-based chronological review (1995-2004) of research on Phytophthora ramorum, the causal agent of sudden oak death. Phytopathol. Mediterr. 44:127-143.
46. Garbelotto M, Schmidt D. 2009. Phosphonate controls sudden oak death pathogen for up to 2 years. Calif. Agric. 63:10-17.
47. Garbelotto M, Svihra P, Rizzo D. 2001. Sudden oak death syndrome fells 3 oak species. Calif. Agric. 55:9-19.
48. Goheen E, et al. 2004. An eradication strategy for Phytophthora ramorum in Oregon coastal forests. Phytopathology 94:S35.
49. Goss EM, Carbone I, Grunwald NJ. 2009. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Mol. Ecol. 18:1161-1174.
50. Goss EM, et al. 2011. Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology 101: 166-171.
51. Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S. 2012. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol. 20:131-138.
52. Grünwald N, Goss E, Press C. 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. 9:729-740.
53. Haas SE, Hooten MB, Rizzo DM, Meentemeyer RK. 2011. Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol. Lett. 14:1108-1116.
54. Hansen EM, Reeser PW, Sutton W, Winton LM, Osterbauer N. 2003. First report of A1 mating type of Phytophthora ramorum in North America. Plant Dis. 87:1267.
55. Hansen E, et al. 2008. Epidemiology of Phytophthora ramorum in Oregon tanoak forests. Can. J. For. Res. 38:1133-1143.
56. Hansen E, Parke J, Sutton W. 2005. Susceptibility of Oregon forest trees and shrubs to Phytophthora ramorum: a comparison of artificial inoculation and natural infection. Plant Dis. 89:63-70.
57. Hansen E, et al. 2003. Phytophthora nemorosa, a new species causing cankers and leaf blight of forest trees in California and Oregon, U. S. A. Mycotaxon 88:129-138.
58. Hansen EM, Reeser PW, Sutton W. 2012. Phytophthora beyond agriculture. Annu. Rev. Phytopathol. 50:359-378.
59. Hardham AR. 2007. Cell biology of plant-oomycete interactions. Cell. Microbiol. 9:31-39.
60. Harnik TY, Mejia-Chang M, Lewis J, Garbelotto M. 2004. Efficacy of heat-based treatments in eliminating the recovery of the sudden oak death pathogen (Phytophthora ramorum) from infected California bay laurel leaves. HortScience 39:1677-1680.
61. Hayden KJ, Lundquist A, Schmidt DJ, Sniezko RA, Frankel SJ, Garbelotto M. 2010. Tanoak resistance: can it be used to sustain populations? p 183-188. In Frankel SJ, Kliejunas JT, PalmieriKM(ed), Proceedings of the Sudden Oak Death Fourth Science Symposium. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, CA.
62. Hayden KJ, Nettel A, Dodd RS, Garbelotto M. 2011. Will all the trees fall? Variable resistance to an introduced forest disease in a highly susceptible host. For. Ecol. Manage. 261:1781-1791.
63. Hayden K, Wright JW, Dodd R, Garbelotto M. Development of a disease resistance research program for tanoaks. In Disease and Insect Resistance in Forest Trees: Proceedings of the 4th International Workshop on the Genetics of Host-Parasite Interactions in Forestry, in press. USDA-Forest Service Pacific Southwest Research Station, Albany, CA.
64. Hüberli D, Garbelotto M. 2012. Phytophthora ramorum is a generalist plant pathogen with differences in virulence between isolates from infectious and dead-end hosts. For. Pathol. 42:8-13.
65. Hüberli D, Hayden KJ, Calver M, Garbelotto M. 2011. Intraspecific variation in host susceptibility and climatic factors mediate epidemics of sudden oak death in western US forests. Plant Pathol. 61:579-592.
66. Ivors K, 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. 15:1493-1505.
67. Ivors K, Hayden K, Bonants P, Rizzo D, Garbelotto M. 2004. AFLP and phylogenetic analyses of North American and European populations of Phytophthora ramorum. Mycol. Res. 108:378-392.
68. Judelson HS, Blanco FA. 2005. The spores of Phytophthora: weapons of the plant destroyer. Nat. Rev. Microbiol. 3:47-58.
69. Jung T, et al. 2003. Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycol. Res. 107:772-789.
70. Kasuga T, et al. 2012. Phenotypic diversification is associated with host-induced transposon derepression in the sudden oak death pathogen Phytophthora ramorum. PLoS One 7:e34728. doi:10.1371/journal. pone.0034728.
71. Kelly M, Meentemeyer R. 2002. Landscape dynamics of the spread of sudden oak death. Photogramm. Eng. Remote Sensing 68:1001-1009.
72. Kozanitas M, Garbelotto M. Long-term monitoring of disease progression and the population genetics of Phytophthora ramourm within the SFPUC watershed in San Mateo County. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
73. Kroon LPNM, Brouwer H, de Cock AWAM, Govers F. 2012. The genus Phytophthora anno 2012. Phytopathology 102:348-364.
74. Kuljian H, Varner JM. 2010. The effects of sudden oak death on foliar moisture content and crown fire potential in tanoak. For. Ecol. Manage. 259:2103-2110.
75. Lane CR, et al. 2003. First outbreak of Phytophthora ramorum in England, on Viburnum tinus. Plant Pathol. 52:414.
76. Linzer R, Rizzo D, Cacciola S, Garbelotto M. 2009. AFLPs detect low genetic diversity for Phytophthora nemorosa and P. pseudosyringae in the US and Europe. Mycol. Res. 113:298-307.
77. Liu D, Kelly M, Gong P, Guo Q. 2007. Characterizing spatial-temporal tree mortality patterns associated with a new forest disease. For. Ecol. Manage. 253:220-231.
78. Maloney P, Lynch S, Kane S, Jensen C, Rizzo D. 2005. Establishment of an emerging generalist pathogen in redwood forest communities. J. Ecol. 93:899-905.
79. Manter DK, Kolodny EH, Hansen EM, Parke JL. 2010. Virulence, sporulation, and elicitin production in three clonal lineages of Phytophthora ramorum. Physiol. Mol. Plant Pathol. 74:317-322.
80. Mascheretti S, Croucher P, Kozanitas M, Baker L, Garbelotto M. 2009. Genetic epidemiology of the sudden oak death pathogen Phytophthora ramorum in California. Mol. Ecol. 18:4577-4590.
81. Mascheretti S, Croucher 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. Mol. Ecol. 17:2755-2768.
82. McPherson B, et al. 2010. Responses of oaks and tanoaks to the sudden oak death pathogen after 8y of monitoring in two coastal California forests. For. Ecol. Manage. 259:2248-2255.
83. McPherson B, et al. 2005. Sudden oak death in California: disease progression in oaks and tanoaks. For. Ecol. Manage. 213:71-89.
84. Meentemeyer R, Anacker B, Mark W, Rizzo D. 2008. Early detection of emerging forest disease using dispersal estimation and ecological niche modeling. Ecol. Appl. 18:377-390.
85. Meentemeyer R, et al. 2008. Impact of sudden oak death on tree mortality in the Big Sur ecoregion of California. Biol. Invasions 10:1243-1255.
86. Meentemeyer RK, et al. 2011. Epidemiological modeling of invasion in heterogeneous landscapes: spread of sudden oak death in California (1990-2030). Ecosphere 2:art17. doi:10.1890/ES10-00192.1.
87. Metz MR, Frangioso KM, Meentemeyer RK, Rizzo DM. 2011. Interacting disturbances: wildfire severity affected by stage of forest disease invasion. Ecol. Appl. 21:313-320.
88. Moralejo E, Descals E. 2011. Diplanetism and microcyclic sporulation in Phytophthora ramorum. For. Pathol. 41:349-354.
89. Moralejo E, Muñoz JAG, Descals E. 2006. Insights into Phytophthora ramorum sporulation: epidemiological and evolutionary implications. EPPO Bulletin 36:383-388.
90. Moralejo E, et al. 2009. Multiple alien Phytophthora taxa discovered on diseased ornamental plants in Spain. Plant Pathol. 58:100-110.
91. Moralejo E, Puig M, García JA, Descals E. 2006. Stromata, sporangiomata and chlamydosori of Phytophthora ramorum on inoculated Mediterranean woody plants. Mycol. Res. 110:1323-1332.
92. Nagle AM, Mcpherson BA, Wood DL, Garbelotto M, Bonello P. 2011. Relationship between field resistance to Phytophthora ramorum and constitutive phenolic chemistry of coast live oak. For. Pathol. 41:464-469.
93. Niklas KJ. 1985. The aerodynamics of wind pollination. Bot. Rev. 51: 328-386.
94. Oak S, Hwang J, Jeffers SJ, Tkacz B. 2008. 2006 pilot survey for Phytophthora ramorum in forest streams in the U. S. A., p 59-64. In Frankel, SJ, Kliejunas, JT, Palmieri, KM (ed), Proceedings of the sudden oak death third science symposium. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, CA.
95. Ockels FS, Eyles A, McPherson BA, Wood DL, Bonello P. 2007. Phenolic chemistry of coast live oak response to Phytophthora ramorum infection. J. Chem. Ecol. 33:1721-1732.
96. Parke J, et al. 2007. Phytophthora ramorum colonizes tanoak xylem and is associated with reduced stem water transport. Phytopathology 97: 1558-1567.
97. Petersen R. 1974. The rust fungus life cycle. Bot. Rev. 40:453-513.
98. Podger FD, Doepel RF, Zentmyer GA. 1965. Association of Phytophthora cinnamomi with a disease of Eucalyptus marginata forest in Western Australia. Plant Dis. Rep. 49:943-947.
99. PRISM Climate Group at Oregon State University. 2012. United States average monthly or annual maximum temperature, 1981-2010. PRISM Climate Group at Oregon State University, Corvallis, OR. www.prism.oregonstate.edu/. Accessed 10 September 2012.
100. Prospero S, Hansen E, Grunwald N, Winton L. 2007. Population dynamics of the sudden oak death pathogen Phytophthora ramorum in Oregon from 2001 to 2004. Mol. Ecol. 16:2958-2973.
101. Prospero S, Grünwald NJ, Winton LM, Hansen EM. 2009. Migration patterns of the emerging plant pathogen Phytophthora ramorumon the West Coast of the United States of America. Phytopathology 99:739-749.
102. Ramage BS, Forrestel AB, Moritz MA, O'Hara KL. 2012. Sudden oak death disease progression across two forest types and spatial scales. J. Veg. Sci. 23:151-163.
103. Ramage BS, O'Hara KL, Forrestel AB. 2011. Forest transformation resulting from an exotic pathogen: regeneration and tanoak mortality in coast redwood stands affected by sudden oak death. Can. J. For. Res. 41:763-772.
104. 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. 86:205-214.
105. 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. 43:309-335.
106. Rizzo D, Garbelotto M. 2003. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1:197-204.
107. Shishkoff N. 2007. Persistence of Phytophthora ramorum in soil mix and roots of nursery ornamentals. Plant Dis. 91:1245-1249.
108. Stamm E, Parke J. The effect of Phytophthora ramorum on the physiology and xylem function of young tanoak trees. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDA-Forest Service, Albany, CA, in press.
109. Swain S, et al. 2006. Composting is an effective treatment option for sanitization of Phytophthora ramorum-infected plant material. J. Appl. Microbiol. 101:815-827.
110. Swiecki TJ, Bernhardt E. Diagnosis and management of Phytophthora ramorumin canyon live oak, an atypical bole canker host. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDAForest Service, Albany, CA, in press.
111. Tooley PW, Browning M. 2008. Survival of Phytophthora ramorum chlamydospores at high and low temperatures, p 475. In Proceedings of the sudden oak death third science symposium. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, CA.
112. Tooley P, Browning M, Berner D. 2008. Recovery of Phytophthora ramorum following exposure to temperature extremes. Plant Dis. 92: 431-437.
113. Tooley P, Browning M, Kyde K, Berner D. 2009. Effect of temperature and moisture period on infection of Rhododendron "Cunningham's White" by Phytophthora ramorum. Phytopathology 99:1045-1052.
114. Tooley P, Kyde K, Englander L. 2004. Susceptibility of selected ericaceous ornamental host species to Phytophthora ramorum. Plant Dis. 88: 993-999.
115. Tyler B, et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261-1266.
116. Valachovic YS, et al. 2011. Sudden oak death-caused changes to surface fuel loading and potential fire behavior in Douglas-fir-tanoak forests. For. Ecol. Manage. 261:1973-1986.
117. Van Poucke K, Heungens K, Franceschini S, Webber J, Brasier C. Phytophthora ramorum in Europe: a research update. In Frankel SJ, Palmieri KM, Alexander J (ed), Proceedings of the Fifth Sudden Oak Death Science Symposium, 19 to 22 June 2012, Petaluma, CA. USDAForest Service, Albany, CA, in press.
118. Vercauteren A, et al. 2010. Clonal expansion of the Belgian Phytophthora ramorum populations based on new microsatellite markers. Mol. Ecol. 19:92-107.
119. Vercauteren A, et al. 2011. Aberrant genome size and instability of Phytophthora ramorum oospore progenies. Fungal Genet. Biol. 48:537-543.
120. Vettraino AM, Hüberli D, Garbelotto M. 2008. Phytophthora ramorum infection of coast live oak leaves in Californian forests and its capacity to sporulate in vitro. Australas. Plant Pathol. 37:72-73.
121. Waring K, O'Hara K. 2008. Redwood/tanoak stand development and response to tanoak mortality caused by Phytophthora ramorum. For. Ecol. Manage. 255:2650-2658.
122. 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. 22:19.
123. Werres S, Marwitz R. 1997. Unbekannte Phytophthora. Deutscher Gartenbau 21:1166-1168.
124. Werres S, et al. 2001. Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycol. Res. 105:1155-1165.
125. Werres S, Zielke B. 2003. First studies on the pairing of Phytophthora ramorum. Z. Pflanzenk. Pflanzen. 110:129-130.
126. Werres S, De Merlier D. 2003. First detection of Phytophthora ramorum mating type A2 in Europe. Plant Dis. 87:1266.
127. Wickland A, Jensen C, Rizzo D. 2008. Geographic distribution, disease symptoms and pathogenicity of Phytophthora nemorosa and Phytophthora pseudosyringae in California, U. S. A. Forest Pathol. 38:288-298.
128. Widmer TL. 2009. Infective potential of sporangia and zoospores of Phytophthora ramorum. Plant Dis. 93:30-35.