Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2

Fungal Biology

Volumn 116, Issue 11, 2012, Pages 1178-1191

  Van Poucke, Kris ^a   Franceschini, Selma ^b   Webber, Joan F ^b   Vercauteren, Annelies ^a,e   Turner, Judith A ^c   McCracken, Alistair R ^d   Heungens, Kurt ^a   Brasier, Clive M ^b  

^a INSTITUTE FOR AGRICULTURAL AND FISHERIES RESEARCH ILVO   (Belgium)

^b FOREST RESEARCH   (United Kingdom)

^c FOOD AND ENVIRONMENT RESEARCH AGENCY   (United Kingdom)

^d AGRI FOOD AND BIOSCIENCES INSTITUTE   (United Kingdom)

^e CropDesign NV   (Belgium)

Author keywords

Introduced pathogen; Larch; Oomycete; PCR RFLP; Plant health

Indexed keywords

CYTOCHROME C OXIDASE; DNA; RIBOSOMAL SPACER DNA; TUBULIN;

AGGRESSION; DECIDUOUS TREE; FOREST ECOSYSTEM; FUNGUS; MORTALITY; OUTCROSSING; PATHOGENICITY; POLYMERASE CHAIN REACTION; POLYMORPHISM;

ARTICLE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FUNGAL GENE; GENETIC VARIABILITY; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYTOPHTHORA; PLANT DISEASE; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEQUENCE ALIGNMENT; TREE; UNITED KINGDOM; UNITED STATES;

BASE SEQUENCE; DNA; DNA, RIBOSOMAL SPACER; ELECTRON TRANSPORT COMPLEX IV; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; NORTHERN IRELAND; PHYLOGENY; PHYTOPHTHORA; PLANT DISEASES; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SCOTLAND; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TREES; TUBULIN; UNITED STATES;

IRELAND; SCOTLAND; UNITED KINGDOM; UNITED STATES;

CAMELLIA; LARIX; LITHOCARPUS; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA RAMORUM; PSEUDOLARIX KAEMPFERI; RHODODENDRON; VIBURNUM;

EID: 84869145529     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2012.09.003     Document Type: Article

References (60)

1. Anon Scientific opinion on the pest risk analysis on Phytophthora ramorum prepared by the FP6 project RAPRA. EFSA Journal 2011, 9:2186-2294. 10.2903/j.efsa.2011.2186.
2. Bayer R.J., Mabberley D.J., Morton C., Miller C.H., Sharma I.K., Pfeil B.E., Rich S., Hitchcock R., Sykes S. A molecular phylogeny of the orange subfamily (Rutaceae: Aurantioideae) using nine cpDNA sequences. American Journal of Botany 2009, 96:668-685.
3. Blair J.E., Coffey M.D., Park S., Geiser D.M., Kang S. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 2008, 45:266-277.
4. Boutet X., Laurent F., Chandelier A. Influence of the medium-solidifying agent, the nutrient, and the genotype on the production of gametangia by Phytophthora ramorum in vitro. Mycological Research 2009, 113:110-116.
5. Boutet X., Vercauteren A., Heungens K., Laurent F., Chandelier A. Oospore progenies from Phytophthora ramorum. Fungal Biology 2010, 114:369-378.
6. Brasier C, 1967. Physiology of reproduction in Phytophthora. PhD thesis, University of Hull.
7. Brasier C.M. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 2008, 57:792-808.
8. Brasier C., Kirk S. Production of gametangia by Phytophthora ramorum in vitro. Mycological Research 2004, 108:823-827.
9. Brasier C.M., Denman S., Brown A., Webber J.F. Sudden oak death (Phytophthora ramorum) discovered on trees in Europe. Mycological Research 2004, 108:1107-1110.
10. Brasier C., Webber J. Sudden larch death. Nature 2010, 466:824-825.
11. Brasier C.M., Beales P.A., Kirk S.A., Denman S., Rose J. Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in Britain. Mycological Research 2005, 109:1-7.
12. Brasier C., Kirk S., Rose J. 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. Proceedings of the Third International IUFRO Working Party 2006, 166-173. Forest Research, Farnham, UK. C.M. Brasier, T. Jung, W. Oßwald (Eds.).
13. Brasier C.M., Kirk S.A., Rose J. Adaptive differences between Phytophthora ramorum isolates from Europe and North America: evidence for separate subspecies?. Proceedings of the Sudden Oak Death Second Science Symposium: the state of our knowledge 2006, 101-103. USDA Forest Research Pacific South West General Technical Report 196, Albany, CA. S.J. Frankel, P.J. Shea, M.I. Haverty (Eds.).
14. Brasier C.M., Vettraino A.M., Chang T.T., Vannini A. Phytophthora lateralis discovered in an old growth Chamaecyparis forest in Taiwan. Plant Pathology 2010, 59:595-603.
15. Cooke D.E.L., Drenth A., Duncan J.M., Wagels G., Brasier C.M. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 2000, 30:17-32.
16. Denman S., Kirk S.A., Moralejo E., Webber J.F. Phytophthora ramorum and P. kernoviae on naturally infected asymptomatic foliage. EPPO Bulletin 2009, 39:105-111.
17. Dieringer D., Schlötterer C. MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 2003, 3:167-169.
18. Donahoo R., Blomquist C.L., Thomas S.L., Moulton J.K., Cooke D.E.L., Lamour K.H. Phytophthora foliorum sp. nov., a new species causing leaf blight of azalea. Mycological Research 2006, 110:1309-1322.
19. Elliott C.G., Hendrie M.R., Knights B.A. The sterol requirement of Phytophthora cactorum. Journal of General Microbiology 1966, 42:425-435.
20. Elliott M., Sumampong G., Varga A., Shamoun S.F., James D., Masri S., Briere S.C., Grünwald N.J. PCR-RFLP markers identify three lineages of the North American and European populations of Phytophthora ramorum. Forest Pathology 2009, 39:266-278.
21. Elliott M., Sumampong G., Varga A., Shamoun S.F., James D., Masri S., Grünwald N.J. Phenotypic differences among three clonal lineages of Phytophthora ramorum. Forest Pathology 2011, 41:7-14.
22. Erwin D.C., Ribeiro O.K. Phytophthora Diseases Worldwide 1996, APS Press, St Paul, MN.
23. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.6 2004, Department of Genomic Sciences, University of Washington, Seattle, WA.
24. Fichtner E.J., Rizzo D.M., Kirk S.A., Webber J.F. Root infections may challenge management of invasive Phytophthora spp. in UK woodlands. Plant Disease 2011, 95:13-18.
25. Frankel S.J. Sudden oak death and Phytophthora ramorum in the USA: a management challenge. Australasian Plant Pathology 2008, 37:19-25.
26. Goss E.M., Carbone I., Grünwald N.J. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Molecular Ecology 2009, 18:1161-1174.
27. Goss E.M., Larsen M., Chastagner G.A., Givens D.R., Grünwald N.J. Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Pathogens 2009, 5:e1000583. 10.1371/journal.ppat.1000583.
28. Goss E.M., Larsen M., Vercauteren A., Werres S., Heungens K., Grünwald N.J. Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology 2011, 101:166-171.
29. Grünwald N.J., Goss E.M., Ivors K., Garbelotto M., Martin F.N., Prospero S., Hansen E., Bonants P.J.M., Hamelin R.C., Chastagner G., Werres S., Rizzo D.M., Abad G., Beales P., Bilodeau G.J., Blomquist C.L., Brasier C., Briere S.C., Chandelier A., Davidson J.M., Denman S., Elliott M., Frankel S.J., Goheen E.M., de Gruyter H., Heungens K., James D., Kanaskie A., McWilliams M.G., in 't Veld W.M., Moralejo E., Osterbauer N.K., Palm M.E., Parke J.L., Sierra A.M.P., Shamoun S.F., Shishkoff N., Tooley P.W., Vettraino A.M., Webber J., Widmer T.L. Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology 2009, 99:792-795.
30. Grünwald N.J., Goss E.M., Press C.M. 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 2008, 9:729-740.
31. Grünwald N.J., Garbelotto M., Goss E.M., Heungens K., Prospero S. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends in Microbiology 2012, 20:131-138.
32. Hall T. Bioedit v5.0.6 2001, Department of Microbiology, North Carolina State University. http://www.mbio.ncsu.edu/BioEdit/bioedit.html.
33. Hüberli D., Harnik T.Y., Meshriy M., Miles L., Garbelotto M. Phenotypic variation among Phytophthora ramorum isolates from California and Oregon. Proceedings of the Sudden Oak Death Second Science Symposium: the state of our knowledge 2006, 131-134. USDA Forest Research Service Pacific South West General Technical Report 196, Albany, CA. S.J. Frankel, P.J. Shea, M.I. Haverty (Eds.).
34. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
35. Ivors K.L., Garbelotto M., Vries I.D.E., Ruyter-Spira C., Hekkert B.T., Rosenzweig N., Bonants P. Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Molecular Ecology 2006, 15:1493-1505.
36. Ivors K.L., Hayden K.J., Bonants P.J.M., Rizzo D.M., Garbelotto M. AFLP and phylogenetic analyses of North American and European populations of Phytophthora ramorum. Mycological Research 2004, 108:378-392.
37. Jiang R.H.Y., Tripathy S., Govers F., Tyler B.M. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences 2008, 105:4874-4879.
38. Kroon L.P.N.M., Bakker F.T., van den Bosch G.B.M., Bonants P.J.M., Flier W.G. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 2003, 41:766-782.
39. Kroon L.P.N.M., Verstappen E.C.P., Kox L.F.F., Flier W.G., Bonants P.J.M. A rapid diagnostic test to distinguish between American and European populations of Phytophthora ramorum. Phytopathology 2004, 94:613-620.
40. Martin F.N. Mitochondrial haplotype determination in the oomycete plant pathogen Phytophthora ramorum. Current Genetics 2008, 54:23-34.
41. Martin F.N., Tooley P.W. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 2003, 95:269-284.
42. Mascheretti S., Croucher P.J.P., Vettraino A., Prospero S., Garbelotto M. Reconstruction of the sudden oak death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum. Molecular Ecology 2008, 17:2755-2768.
43. Nei M., Tajima F., Tateno Y. Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution 1983, 19:153-170.
44. Prospero S., Black J.A., Winton L.M. Isolation and characterization of microsatellite markers in Phytophthora ramorum, the causal agent of sudden oak death. Molecular Ecology Notes 2004, 4:672-674.
45. Prospero S., Hansen E.M., Grünwald N.J., Winton L.M. Population dynamics of the sudden oak death pathogen Phytophthora ramorum in Oregon from 2001 to 2004. Molecular Ecology 2007, 16:2958-2973.
46. Rizzo D.M., Garbelotto M., Davidson J.M., Slaughter G.W., Koike S.T. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease 2002, 86:205-214.
47. Ronquist F., Huelsenbeck J.P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
48. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
49. Tyler B.M., Tripathy S., Zhang X.M., Dehal P., Jiang R.H.Y., Aerts A., Arredondo F.D., Baxter L., Bensasson D., Beynon J.L., Chapman J., Damasceno C.M.B., Dorrance A.E., Dou D.L., Dickerman A.W., Dubchak I.L., Garbelotto M., Gijzen M., Gordon S.G., Govers F., Grünwald N.J., Huang W., Ivors K.L., Jones R.W., Kamoun S., Krampis K., Lamour K.H., Lee M.K., McDonald W.H., Medina M., Meijer H.J.G., Nordberg E.K., Maclean D.J., Ospina-Giraldo M.D., Morris P.F., Phuntumart V., Putnam N.H., Rash S., Rose J.K.C., Sakihama Y., Salamov A.A., Savidor A., Scheuring C.F., Smith B.M., Sobral B.W.S., Terry A., Torto-Alalibo T.A., Win J., Xu Z.Y., Zhang H.B., Grigoriev I.V., Rokhsar D.S., Boore J.L. Phytophthora genome sequences uncover evolutionary origins and methods of pathogenesis. Science 2006, 313:1261-1266.
50. Vercauteren A., Boutet X., D'hondt L., Van Bockstaele E., Maes M., Leus L., Chandelier A., Heungens K. Aberrant genome size and instability of Phytophthora ramorum oospore progenies. Fungal Genetics and Biology 2011, 48:537-543.
51. Vercauteren A., De Dobbelaere I., Grünwald N.J., Bonants P., Van Bockstaele E., Maes M., Heungens K. Clonal expansion of the Belgian Phytophthora ramorum populations based on new microsatellite markers. Molecular Ecology 2010, 19:92-107.
52. Vercauteren A., De Dobbelaere I., Van Bockstaele E., Maes M., Heungens K. Genotypic and phenotypic characterization of the European A2 isolates of Phytophthora ramorum. European Journal of Plant Pathology 2011, 129:621-635.
53. Vercauteren A., Larsen M., Goss E.M., Grünwald N.J., Maes M., Heungens K. Identification of new polymorphic microsatellite markers in the NA1 and NA2 lineages of Phytophthora ramorum. Mycologia 2011, 103:1245-1249.
54. Vercauteren A, Riedel M, Maes M, Werres S, Heungens K. Survival of Phytophthora ramorum in Rhododendron root balls and in rootless substrates. Plant Pathology 61, in press, doi:10.1111/j.1365-3059.2012.02627.x.
55. Vincze T., Posfai J., Roberts R.J. NEBcutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Research 2003, 31:3688-3691.
56. Webber J.F. Status of Phytophthora ramorum and P. kernoviae in Europe. Proceedings of the Sudden Oak Death Third Science Symposium 2008, 195-198. USDA Forest Service Pacific South West General Technical Report 214, Albany, CA. S.J. Frankel, J.T. Kliejunas, K.M. Palmieri (Eds.).
57. Webber J.F., Mullett M., Brasier C.M. Dieback and mortality of plantation Japanese larch (Larix kaempferi) associated with infection by Phytophthora ramorum. New Disease Reports 2010, 22:19.
58. Werres S., Kaminski K. Characterisation of European and North American Phytophthora ramorum isolates due to their morphology and mating behaviour in vitro with heterothallic Phytophthora species. Mycological Research 2005, 109:860-871.
59. Werres S., Marwitz R., Veld W.A.M.I., De Cock A.W.A.M., Bonants P.J.M., De Weerdt M., Themann K., Ilieva E., Baayen R.P. Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycological Research 2001, 105:1155-1165.
60. White T.J., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a guide to methods and applications 1990, 315-322. Academic Press, San Diego, CA. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).