, Volume 249, Issue 1, pp 3–19 | Cite as

The evolutionary phylogeny of the oomycete “fungi”

  • Gordon W. BeakesEmail author
  • Sally L. Glockling
  • Satoshi Sekimoto
Review Article


Molecular sequencing has helped resolve the phylogenetic relationships amongst the diverse groups of algal, fungal-like and protist organisms that constitute the Chromalveolate “superkingdom” clade. It is thought that the whole clade evolved from a photosynthetic ancestor and that there have been at least three independent plastid losses during their evolutionary history. The fungal-like oomycetes and hyphochytrids, together with the marine flagellates Pirsonia and Developayella, form part of the clade defined by Cavalier-Smith and Chao (2006) as the phylum “Pseudofungi”, which is a sister to the photosynthetic chromistan algae (phylum Ochrophyta). Within the oomycetes, a number of predominantly marine holocarpic genera appear to diverge before the main “saprolegnian” and “peronosporalean” lines, into which all oomycetes had been traditionally placed. It is now clear that oomycetes have their evolutionary roots in the sea. The earliest diverging oomycete genera so far documented, Eurychasma and Haptoglossa, are both obligate parasites that show a high degree of complexity and sophistication in their host parasite interactions and infection structures. Key morphological and cytological features of the oomycetes will be reviewed in the context of our revised understanding of their likely phylogeny. Recent genomic studies have revealed a number of intriguing similarities in host–pathogen interactions between the oomycetes with their distant apicocomplexan cousins. Therefore, the earlier view that oomycetes evolved from the largely saprotrophic “saprolegnian line” is not supported and current evidence shows these organisms evolved from simple holocarpic marine parasites. Both the hyphal-like pattern of growth and the acquisition of oogamous sexual reproduction probably developed largely after the migration of these organisms from the sea to land.


Apicocomplexa Chromalveolates Eurychasma Haliphthoros Olpidiopsis Oomycetes Pathogenicity Phylogeny Ultrastructure 



Dense-body vesicle


Encystment vesicle


Fingerprint vesicle


Parasitophorous vacuolar membrane


Transitional helix



Our special thanks are extended to Daiske Honda who mentored and guided the work on the marine parasites which formed part of doctoral thesis of SS and our many colleagues who have shared their phylogenetic data with us.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Adl SM et al (2005) The new higher level classification of the eukaryotes with emphasis on the taxonomy of protists. J Eukary Microbiol 52:399–451CrossRefGoogle Scholar
  2. Bala K, Robideau GP, Lévesque A, de Cock AWAM, Abad ZG, Lodhi AM, Shahzad S, Ghaffar A, Coffey MD (2010) Phytopythium gen. nov. and Phytopythium sindhum sp. nov. Persoonia 24:36–137Google Scholar
  3. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977PubMedCrossRefGoogle Scholar
  4. Barr DJS, Allan PME (1985) Comparison of the flagellar apparatus in Phytophthora, Saprolegnia, Thraustochytrium and Rhizidiomyces. Can J Bot 63:138–154CrossRefGoogle Scholar
  5. Barr DJS, Désaulniers NL (1987) Ultrastructure of the Lagena radicola zoospore, including a comparison with the primary and secondary Saprolegnia zoospores. Can J Bot 65:2161–2176CrossRefGoogle Scholar
  6. Barr DJS, Désaulniers NL (1992) The flagellar apparatus of Phytophthora Pythium and Halophytophthora. Can J Bot 70:2163–2169CrossRefGoogle Scholar
  7. Barstow WE, Freshour GD, Fuller MS (1989) The ultrastructure of mitosis during zoosporogenesis in Rhizidiomyces apophysatus. Can J Bot 67:3401–3409CrossRefGoogle Scholar
  8. Bartnick-Garcia S, Wang MC (1983) Biochemical aspects of morphogenesis in Phytophthora. In Phytophthora. Its biology,taxonomy, ecology and pathology. eds Erwin DC, Bartnicki-Garcia S, Tsoa PH. St Paul Minnesota, American Phytopathological Society pp 121–137Google Scholar
  9. Beakes GW (1981) Ultrastructural aspects of oospore differentiation. In: The fungal spore: morphogenetic controls. Hohl H, Turian G (eds). Academic Press: London. pp. 71–94Google Scholar
  10. Beakes GW (1987) Oomycete phylogeny: ultrastructural perspectives. In: Evolutionary biology of the fungi. Rayner ADM, Brasier CM, Moore D (eds) Cambridge University Press: Cambridge. pp 405–421Google Scholar
  11. Beakes GW (1989) Oomycete fungi: their phylogeny and relationship to chromophyte algae. In: The chromophyte algae: problems and perspectives. Green JP, Leadbeater BSC, Diver WL (eds). Clarendon Press: Oxford. pp 325–342Google Scholar
  12. Beakes GW, Glockling SL (1998) Injection tube differentiation in gun cells of a Haptoglossa species which infects nematodes. Fungal Genet Biol 24:45–68PubMedCrossRefGoogle Scholar
  13. Beakes GW, Glockling SL (2000) An ultrastructural analysis of organelle arrangement during gun (infection) cell differentiation in the nematode parasite Haptoglossa dickii. Mycol Res 104:1258–1269CrossRefGoogle Scholar
  14. Beakes GW, Glockling SL (2002) A comparative fine-structural study of dimorphic infection cells in the nematophagous parasite Haptoglossa erumpens. Fungal Genet Biol 37:250–262PubMedCrossRefGoogle Scholar
  15. Beakes GW, Sekimoto S (2009) The evolutionary phylogeny of oomycetes—insights gained from studies of holocarpic parasites of algae and invertebrates. In: Oomycete genetics and genomics: diversity, interactions and research tools. Lamour K, Kamoun S (eds) Wiley: New York. pp 1–24.Google Scholar
  16. Beakes GW, Glockling SL, James TY (2006). The diversity of oomycete pathogens of nematodes and its implications to our understanding of oomycete phylogeny. In: Proceedings of the Eighth International Mycological Congress. Meyer W, Pearce C (eds). Medimond: Italy. pp 7–12Google Scholar
  17. Bhattacharjee S, Hiller NL, Konstantinos L, Win J, Thirumala-Devi K, Young C, Kamoun S, Haldar K (2006) The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogen 2(5):e50. doi: 10.1371/journal.ppat.0020050 CrossRefGoogle Scholar
  18. Blair JE, Coffey MD, Park S-Y, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45:266–277PubMedCrossRefGoogle Scholar
  19. Bortnick RN, Powell MJ, Bangert TN (1985) Zoospore fine-structure of the parasite Olpidiopsis saprolegniae (Oomycetes, Lagenidiales). Mycologia 77:861–879CrossRefGoogle Scholar
  20. Brasier C, Weber J (2010) Sudden larch death. Nature 466:824–825PubMedCrossRefGoogle Scholar
  21. Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biol Lett 4:366–369PubMedCrossRefGoogle Scholar
  22. Burr AW, Beakes GW (1994) Characterization of zoospore and cyst surface structure in saprophytic and fish pathogenic Saprolegnia species (oomycete fungal protists). Protoplasma 181:142–163CrossRefGoogle Scholar
  23. Cavalier-Smith T, Chao EEY (2006) Phylogeny and megasystematics of phagotrophic heterokonts (Kingdom Chromista). J Mol Evolution 62:388–420CrossRefGoogle Scholar
  24. Cook KL, Hudspeth DSS, Hudspeth MES (2001) A cox2 phylogeny of representative marine peronosporomycetes (Oomycetes). Nova Hedwig 122:231–243Google Scholar
  25. Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32PubMedCrossRefGoogle Scholar
  26. Dearnaley JDW, Maleszka J, Hardham AR (1996) Synthesis of zoospore peripheral vesicles during sporulation of Phytophthora cinnamomi. Mycol Res 100:39–48CrossRefGoogle Scholar
  27. Dick MW (2001) Straminipilous fungi. Kluwer Academic Publishers, Dordrecht, 670 ppGoogle Scholar
  28. Dykstra MJ, Noga EJ, Levine JF, Moye DW, Hawkins JH (1986) Characterization of the Aphanomyces species involved with ulcerative mycosis (UM) in menhaden. Mycologia 78:664–672CrossRefGoogle Scholar
  29. Gachon CMM, Strittmatter M, Muller DG, Kleintech J, Kupper FC (2009) Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Appl Envir Microbiol 75:322–328. doi: 10.1128/AEM.01885-08 CrossRefGoogle Scholar
  30. Gaulin E, Madoui A-M, Bottin A, Jacquet C, Mathe C, Couloux A, Wincker P, Dumas B (2008) Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenecity factors and metabolic pathways. PlosOne. doi: 10.1371/journal.pone.0001723 Google Scholar
  31. Glockling SL, Beakes GW (2000a) Two new Haptoglossa species (H. erumpens and H. dickii) infecting nematodes in cow manure. Mycol Res 104:100–106CrossRefGoogle Scholar
  32. Glockling SL, Beakes GW (2000b) The ultrastructure of the dimorphic infection cells of Haptoglossa heteromorpha illustrates the developmental plasticity of infection apparatus structures in a nematode parasite. Can J Botany 78:1095–1107CrossRefGoogle Scholar
  33. Glockling SL, Beakes GW (2000c) An ultrastructural study of sporidium formation during infection of a rhabditid nematode by large gun cells of Haptoglossa heteromorpha. J Invert Pathol 76:208–215CrossRefGoogle Scholar
  34. Glockling SL, Beakes GW (2000d) A review of the biology and infection strategies of biflagellate zoosporic parasites of nematodes. Fungal Diversity 4:1–20Google Scholar
  35. Glockling SL, Beakes GW (2001) Two new species of Haptoglossa from N.E. England, H. northumbrica and H. polymorpha. Bot J Linn Soc 136:329–338CrossRefGoogle Scholar
  36. Glockling SL, Beakes GW (2006a) Structural and developmental studies of Chlamydomyzium oviparasiticum from Rhabditis nematodes and in culture. Mycol Res 110:1119–1126PubMedCrossRefGoogle Scholar
  37. Glockling SL, Beakes GW (2006b) An ultrastructural study of development and reproduction in the nematode parasite Myzocytiopsis vermicola. Mycologia 98:7–21CrossRefGoogle Scholar
  38. Göker M, Voglmayr H, Riethmüller A, Oberwinkler F (2007) How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genet Biol 44:105–122PubMedCrossRefGoogle Scholar
  39. Gotelli D, Hanson LC (1987) An ultrastructural investigation of the zoospore of Sapromyces androgynus (Oomycetes, Lagenidiales). Mycologia 78:810–817Google Scholar
  40. Grouffaud S, van West P, Avrova AO, Birch PRJ, Whisson SC (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154:3743–3751PubMedCrossRefGoogle Scholar
  41. Gubler F, Hardham AR (1988) Secretion of adhesive material during encystement of Phytophthora cinnamomi zoospores characterized by immunogold labeling with monoclonal antibodies to components of peripheral vescicles. J Cell Science 90:225–235Google Scholar
  42. Haas BJ, Kamoun S et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398. doi: 10.1038/nature08358 PubMedCrossRefGoogle Scholar
  43. Hakariya M, Masuyama N, Saikawa M (2002) Shooting of sporidium by "gun" cells in Haptoglossa heterospora and H. zoospora and secondary zoospore formation in H. zoospora. Mycoscience 43:119–125CrossRefGoogle Scholar
  44. Hakariya M, Hirose D, Tokumasu S (2007) A molecular phylogeny of Haptoglossa species, terrestrial peronosporomycetes (oomycetes) endoparasitic on nematodes. Mycoscience 48:169–175CrossRefGoogle Scholar
  45. Hakariya M, Hirose D, Tokumasu S (2009) Molecular phylogeny of terrestrial holocarpic endoparasitic peronosporomycetes, Haptoglossa spp. Inferred from 18S rDNA. Mycoscience 50:130–136. doi: 10.1007/s10267-008-0458-9 CrossRefGoogle Scholar
  46. Hardham AR (1987) Microtubules and the flagellar apparatus in zoospores and cysts of the fungus Phytophthora cinnamorni. Protoplasma 137:109–124CrossRefGoogle Scholar
  47. Hardham AR (2005) Pathogen profile: Phytophthora cinnamomi. Mol Plant Path 6:598–604. doi: 10.1111/j.1364-3703,2005.00308.X CrossRefGoogle Scholar
  48. Harper JT, Waanders E, Keeling PJ (2005) On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Sys Evol Microbiol 55:487–496CrossRefGoogle Scholar
  49. Heath IB, Greenwood AD (1970) Centriole replication and nuclear division in Saprolegnia. J Gen Microbiol 62:139–289Google Scholar
  50. Hudspeth DSS, Nadler SA, Hudspeth MES (2000) A cox II molecular phylogeny of the Peronosporomycetes. Mycologia 92:674–684CrossRefGoogle Scholar
  51. Hudspeth DSS, Stenger D, Hudspeth MES (2003) A cox2 phylogenetic hyphothesis for the downy mildews and white rusts. Fungal Diversity 13:47–57Google Scholar
  52. Inaba S, Haryama S (2006) The phylogenetic studies on the genus Cornumyces (Oomycetes) based on the nucleotide sequences of the nuclear large subunit ribosomal RNA and the mitochondrially-encoded cox2 genes. Eighth International Mycological Congress. Congress Handbook and Abstracts. p. 330.Google Scholar
  53. Karling JS (1981) Predominantly holocarpic and eucarpic simple biflagellate phycomycetes. J Cramer, Vaduz, 252 ppGoogle Scholar
  54. Koldziej K, Stoeck T (2007) Cellular identification of a novel uncultured marine stramenopile (MAST-12 Clade) small-subunit rRNA gene sequence from a Norwegian estuary by ues of fluorescence in situ hybridization-scanning electron microscopy. Appl Env Microbiol 73:2718–2726. doi: 10.1128/AEM.02158-06 CrossRefGoogle Scholar
  55. Kühn SF, Medlin LK, Eller G (2004) Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. Protist 155:143–156PubMedCrossRefGoogle Scholar
  56. Küpper FC, Müller DG (1999) Massive occurrence of the heterokont and fungal parasites Anisolpidium, Eurychasma and Chytridium in Pylaiella litoralis (Ectocarpales, Phaeophyceae). Nova Hedwig 69:381–389Google Scholar
  57. Küpper FC, Maier I, Müller DG, Loiseaux-de Goer S, Guillou L (2006) Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Cohn. Cryptogamie Algologie 27:165–184Google Scholar
  58. Lamour KH, Win J, Kamoun S (2007) Oomycete genomics: new insights and future directions. FEMS Microbiol Lett 274:1–8PubMedCrossRefGoogle Scholar
  59. Lehnen LP, Powell MJ (1989) The role of kinetosome-associated organelles in the attachment of encysting secondary zoospores of Saprolegnia ferax to substrates. Protoplasma 149:163–174CrossRefGoogle Scholar
  60. Leipe DD, Tong SM, Goggin CL, Slemenda SB, Pieniazek NJ, Sogin ML (1994) 16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group. Eur J Protistology 33:369–377Google Scholar
  61. Lévesque A et al (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11:R73. doi: 10.1186/gb-2010-11-7-r73 PubMedCrossRefGoogle Scholar
  62. Maréchal E, Cesbron-Delauw M-F (2001) The apicoplast: a new member of the plastid family. Trends Plant Sci 6:1360–1385CrossRefGoogle Scholar
  63. Martin RW, Miller CE (1986) Ultrastructure of mitosis in the endoparasite Olpidiopsis varians. Mycologia 78:11–21CrossRefGoogle Scholar
  64. Massana R, Castresana J, Balagué V, Guillou L, Romari K, Groisillier A, Valentin K, Pedró-Alió C (2004) Phylogenetic and ecological analysis of novel marine stramenopiles. App Env Microbiol 70:3528–3534CrossRefGoogle Scholar
  65. Massana R, Terrado R, Forn I, Lovejoy C, Pedró-Alió C (2006) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Env Microbiol 8:1515–1522CrossRefGoogle Scholar
  66. Müller DG, Küpper FC, Küpper H (1999) Infection experiments reveal broad host ranges of Eurychasma dicksonii (Oomycota) and Chytridium polysiphoniae (Chytridiomycota), two eukaryotic parasites in marine brown algae (Phaeophyceae). Phycological Research 47:217–223CrossRefGoogle Scholar
  67. Nakagiri A (2002) Diversity and phylogeny of Halophytophthora (Oomycetes). Abstracts, 7th International Mycological Congress, Oslo. 55 p.19.Google Scholar
  68. Newell SY, Cefalu R, Fell JW (1977) Myzocytium, Haptoglossa and Gonimochaete (fungi) in littoral marine nematodes. Bull Marine Science 27:197–207Google Scholar
  69. Overton SV, Tharp TP, Bland CE (1983) Fine structure of swimming, encysting, and germinating spores of Haliphthoros milfordensis. Can J Bot 61:1165–1177CrossRefGoogle Scholar
  70. Padgett DE (1978) Observations on the estuarine distribution of Saprolegniceae. Trans Br Mycol Soc 70:41–143CrossRefGoogle Scholar
  71. Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3:1169–1175PubMedCrossRefGoogle Scholar
  72. Petersen AB, Rosendahl S (2000) Phylogeny of the Peronosporomycetes (Oomycota) based on partial sequences of the large ribosomal subunit (LSU rDNA). Mycol Res 104:1295–1303CrossRefGoogle Scholar
  73. Prakob W, Judelson HS (2007) Gene expression during oosporogenesis in heterothallic and homothallic Phytophthora. Fungal Gen Biol 44:726–739CrossRefGoogle Scholar
  74. Pueschel CM, Van der Meer JP (1985) Ultrastructure of the fungus Petersenia palmariae (Oomycota) parasitic on the alga Palmaria molis (Rhodophyceae). Can J Bot 63:409–418CrossRefGoogle Scholar
  75. Raghu Kumar C (1980) An ultrastructural study of the marine diatom Licmophora hyalina and its parasite Ectrogella perforans II. Development of the fungus in its host. Can J Bot 58:2557–2574CrossRefGoogle Scholar
  76. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous pathogens: gene exchange across eukaryote kingdoms. Curr Biol 16:1857–1864PubMedCrossRefGoogle Scholar
  77. Riethmüller A, Weiss M, Oberwinkler F (1999) Phylogenetic studies of Saprolegniomycetidae and related groups based on nuclear large subunit ribosomal DNA sequences. Can J Botany 77:1790–1800CrossRefGoogle Scholar
  78. Riethmüller A, Voglmayr H, Göker M, Weiss M, Oberwinkler F (2002) Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia 94:834–849PubMedCrossRefGoogle Scholar
  79. Robb EJ, Barron GL (1982) Nature’s ballistic missile. Science 218:1221–1222PubMedCrossRefGoogle Scholar
  80. Robold A, Hardham AR (2005) During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr Genet 47:307–315PubMedCrossRefGoogle Scholar
  81. Schnepf E, Deichgräber G, Drebes G (1977) Development and ultrastructure of the marine, parasitic oomcete, Lagenisma coscinodisci (Lagenidiales): sexual reproduction. Can J Bot 56:1315–1325CrossRefGoogle Scholar
  82. Schnepf E, Deichgräber G, Drebes G (1978a) Development and ultrastructure of the marine, parasitic oomycete, Lagenisma coscinodisci Drebes (Lagenidiales). Archiv Microbiol 116:133–139CrossRefGoogle Scholar
  83. Schnepf E, Deichgräber G, Drebes G (1978b) Development and ultrastructure of the marine parasitic oomycete Lagenisma coscinodisci Drebes (Lagenidiales) Thallus, zoosporangium, mitosis and meiosis. Archiv Microbiol 116:121–132Google Scholar
  84. Schnepf E, Deichgräber G, Drebes G (1978c) Development and ultrastructure of the marine, parasitic Oomycete, Lagenisma coscinodisci Drebes (Lagenidiales): formation of the primary zoospores and their release. Protoplasma 94:263–280CrossRefGoogle Scholar
  85. Sekimoto S (2008) The taxonomy and phylogeny of the marine holocarpic oomycetes. Ph.D. Thesis, Graduate School of Natural Sciences, Konan University, Kobe. 195 ppGoogle Scholar
  86. Sekimoto S, Hatai K, Honda D (2007) Molecular phylogeny of an unidentified Haliphthoros-like marine oomycete and Haliphthoros milfordensis inferred from nuclear-encoded small and large subunit rDNA genes and mitochondrial-encoded cox2 gene. Mycoscience 48:212–221CrossRefGoogle Scholar
  87. Sekimoto S, Yokoo K, Kawamura Y, Honda D (2008a) Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, stramenopiles), a unicellular obligate endoparasite of Porphyra spp. (Bangiales, Rhodophyta). Mycol Res 112:361–374PubMedCrossRefGoogle Scholar
  88. Sekimoto S, Beakes GW, Gachon CMM, Müller DG, Küpper FC, Honda D (2008b) The development, ultrastructural cytology, and molecular phylogeny of the basal oomycete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis. Protist 159:401–412CrossRefGoogle Scholar
  89. Sekimoto S, Kochkova TA, West JA, Beakes GW, Honda D (2009) Olpidiopsis bostychiae: a new species endoparasitic oomycete that infects Bostrychia and other red algae. Phycologia 48:460–472. doi: 10.2216/08-11.1 CrossRefGoogle Scholar
  90. Sparrow FK (1960) Aquatic Phycomycetes, 2nd revised edition. University of Michigan Press, Ann Arbor, p 1187Google Scholar
  91. Sparrow FK (1976) The present status of classification in biflagellate fungi. In: Recent advances in aquatic mycology. Gareth-Jones, E.B. (ed). Elek Science: London. pp 213–222Google Scholar
  92. Strittmatter M, Gachon CMM, Kupper F (2009). Ecology of lower oomycetes. In: Oomycete genetics and genomics: diversity, interactions and research tools. Lamour K, Kamoun S (eds). Wiley. pp 25–46.Google Scholar
  93. Strullu-Derrien C, Kenrick P, Rioult JP, Strulli DG (2010) Evidence of parasitic oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern Lyginopteris oldhamia. Proc Royal Soc B. doi: 10.1098/rspb.2010.1603 Google Scholar
  94. Talbot NJ (2007) Deadly special deliveries. Nature 450:41–42PubMedCrossRefGoogle Scholar
  95. Thines M, Voglmayr H (2009). An introduction to the white blister rusts (Albuginales). In: Oomycete genetics and genomics: diversity, interactions and research tools. Lamour K, Kamoun S (eds). Wiley. pp 77–92.Google Scholar
  96. Thines M, Voglmayr H, Göker M, (2009). Taxonomy and phylogeny of the downy mildews (Peronosporaceae). In: Oomycete genetics and genomics: diversity, interactions and research tools. Lamour K, Kamoun S (eds). Wiley. pp 47–75.Google Scholar
  97. Thompson J, Cooke RE, Moore S, Anderson LF, Janse CJ, Waters AP (2004) PTRAMP; a conserved Plasmodium thrombospondin-related apical merozoite protein. Mol Biochem Parasitol 134(2):225–232PubMedCrossRefGoogle Scholar
  98. Torto-Alalibo T, Tian M, Gajendran K, Waugh ME, Van West P, Kamoun S (2005) Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiol 5:46. doi: 1186/1471-2180-5=46 PubMedCrossRefGoogle Scholar
  99. Tsui CKM, Marshall W, Yokoyama R, Honda D, Lippmeier JC, Craven KD, Berbee ML (2006) Labryinthulomycetes phylgeneny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol Phylogenet Evol 50:129–140CrossRefGoogle Scholar
  100. Tyler BM et al (2006) Phytophthora genome sequences uncover the evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266PubMedCrossRefGoogle Scholar
  101. Uzuhashi S, Tojo M, Kakishima M (2010) Phylogeny of the genus Pythium and description of new genera. Mycoscience 51:337–365. doi: 10.1007/s10267-010-0046-7 CrossRefGoogle Scholar
  102. Voglmayer H, Riethmüller A (2006) Phylogenetic relationships of Albugo species (white blister rusts) based on LSU rDNA sequence and oospore data. Mycol Res 110:75–85CrossRefGoogle Scholar
  103. Whisson SC, Boevink PC, Moleleki L et al (2007) A translocation signal for delivery of oomycete effector proteins inside host plant cells. Nature 450:115–118PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Gordon W. Beakes
    • 1
    Email author
  • Sally L. Glockling
    • 3
  • Satoshi Sekimoto
    • 2
  1. 1.School of Biology, Newcastle UniversityNewcastle upon TyneUK
  2. 2.Department of BotanyUniversity of British ColumbiaVancouverCanada
  3. 3.EastbourneUK

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