The evolutionary phylogeny of the oomycete “fungi”

Abstract

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.

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Abbreviations

DBV:

Dense-body vesicle

EV:

Encystment vesicle

FV:

Fingerprint vesicle

PV:

Parasitophorous vacuolar membrane

TH:

Transitional helix

References

  1. Adl SM et al (2005) The new higher level classification of the eukaryotes with emphasis on the taxonomy of protists. J Eukary Microbiol 52:399–451

    Article  Google 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 24:36–137

    Google Scholar 

  3. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977

    PubMed  Article  CAS  Google Scholar 

  4. Barr DJS, Allan PME (1985) Comparison of the flagellar apparatus in Phytophthora, Saprolegnia, Thraustochytrium and Rhizidiomyces. Can J Bot 63:138–154

    Article  Google 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 65:2161–2176

    Article  Google Scholar 

  6. Barr DJS, Désaulniers NL (1992) The flagellar apparatus of Phytophthora Pythium and Halophytophthora. Can J Bot 70:2163–2169

    Article  Google Scholar 

  7. Barstow WE, Freshour GD, Fuller MS (1989) The ultrastructure of mitosis during zoosporogenesis in Rhizidiomyces apophysatus. Can J Bot 67:3401–3409

    Article  Google 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 121–137

  9. Beakes GW (1981) Ultrastructural aspects of oospore differentiation. In: The fungal spore: morphogenetic controls. Hohl H, Turian G (eds). Academic Press: London. pp. 71–94

  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 405–421

  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 325–342

  12. Beakes GW, Glockling SL (1998) Injection tube differentiation in gun cells of a Haptoglossa species which infects nematodes. Fungal Genet Biol 24:45–68

    PubMed  Article  Google 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 104:1258–1269

    Article  Google 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 37:250–262

    PubMed  Article  Google 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.

  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 7–12

  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

    Article  Google 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 45:266–277

    PubMed  Article  CAS  Google Scholar 

  19. Bortnick RN, Powell MJ, Bangert TN (1985) Zoospore fine-structure of the parasite Olpidiopsis saprolegniae (Oomycetes, Lagenidiales). Mycologia 77:861–879

    Article  Google Scholar 

  20. Brasier C, Weber J (2010) Sudden larch death. Nature 466:824–825

    PubMed  Article  CAS  Google Scholar 

  21. Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biol Lett 4:366–369

    PubMed  Article  Google 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 181:142–163

    Article  Google Scholar 

  23. Cavalier-Smith T, Chao EEY (2006) Phylogeny and megasystematics of phagotrophic heterokonts (Kingdom Chromista). J Mol Evolution 62:388–420

    Article  CAS  Google Scholar 

  24. Cook KL, Hudspeth DSS, Hudspeth MES (2001) A cox2 phylogeny of representative marine peronosporomycetes (Oomycetes). Nova Hedwig 122:231–243

    Google Scholar 

  25. Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32

    PubMed  Article  CAS  Google Scholar 

  26. Dearnaley JDW, Maleszka J, Hardham AR (1996) Synthesis of zoospore peripheral vesicles during sporulation of Phytophthora cinnamomi. Mycol Res 100:39–48

    Article  Google Scholar 

  27. Dick MW (2001) Straminipilous fungi. Kluwer Academic Publishers, Dordrecht, 670 pp

    Google 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 78:664–672

    Article  Google 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

    Article  CAS  Google 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 104:100–106

    Article  Google 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 78:1095–1107

    Article  Google 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 76:208–215

    Article  CAS  Google Scholar 

  34. Glockling SL, Beakes GW (2000d) A review of the biology and infection strategies of biflagellate zoosporic parasites of nematodes. Fungal Diversity 4:1–20

    Google 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 136:329–338

    Article  Google Scholar 

  36. Glockling SL, Beakes GW (2006a) Structural and developmental studies of Chlamydomyzium oviparasiticum from Rhabditis nematodes and in culture. Mycol Res 110:1119–1126

    PubMed  Article  Google Scholar 

  37. Glockling SL, Beakes GW (2006b) An ultrastructural study of development and reproduction in the nematode parasite Myzocytiopsis vermicola. Mycologia 98:7–21

    Article  Google 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 44:105–122

    PubMed  Article  Google Scholar 

  39. Gotelli D, Hanson LC (1987) An ultrastructural investigation of the zoospore of Sapromyces androgynus (Oomycetes, Lagenidiales). Mycologia 78:810–817

    Google 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 154:3743–3751

    PubMed  Article  CAS  Google 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 90:225–235

    Google 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

    PubMed  Article  CAS  Google 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 43:119–125

    Article  Google Scholar 

  44. Hakariya M, Hirose D, Tokumasu S (2007) A molecular phylogeny of Haptoglossa species, terrestrial peronosporomycetes (oomycetes) endoparasitic on nematodes. Mycoscience 48:169–175

    Article  CAS  Google 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

    Article  CAS  Google Scholar 

  46. Hardham AR (1987) Microtubules and the flagellar apparatus in zoospores and cysts of the fungus Phytophthora cinnamorni. Protoplasma 137:109–124

    Article  Google Scholar 

  47. Hardham AR (2005) Pathogen profile: Phytophthora cinnamomi. Mol Plant Path 6:598–604. doi:10.1111/j.1364-3703,2005.00308.X

    Article  Google 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 55:487–496

    Article  CAS  Google Scholar 

  49. Heath IB, Greenwood AD (1970) Centriole replication and nuclear division in Saprolegnia. J Gen Microbiol 62:139–289

    Google Scholar 

  50. Hudspeth DSS, Nadler SA, Hudspeth MES (2000) A cox II molecular phylogeny of the Peronosporomycetes. Mycologia 92:674–684

    Article  CAS  Google Scholar 

  51. Hudspeth DSS, Stenger D, Hudspeth MES (2003) A cox2 phylogenetic hyphothesis for the downy mildews and white rusts. Fungal Diversity 13:47–57

    Google 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.

  53. Karling JS (1981) Predominantly holocarpic and eucarpic simple biflagellate phycomycetes. J Cramer, Vaduz, 252 pp

    Google 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

    Article  Google 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 155:143–156

    PubMed  Article  Google 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 69:381–389

    Google 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 27:165–184

    Google Scholar 

  58. Lamour KH, Win J, Kamoun S (2007) Oomycete genomics: new insights and future directions. FEMS Microbiol Lett 274:1–8

    PubMed  Article  CAS  Google 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 149:163–174

    Article  Google 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 33:369–377

    Google 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

    PubMed  Article  Google Scholar 

  62. Maréchal E, Cesbron-Delauw M-F (2001) The apicoplast: a new member of the plastid family. Trends Plant Sci 6:1360–1385

    Article  Google Scholar 

  63. Martin RW, Miller CE (1986) Ultrastructure of mitosis in the endoparasite Olpidiopsis varians. Mycologia 78:11–21

    Article  Google 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 70:3528–3534

    Article  CAS  Google 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 8:1515–1522

    Article  CAS  Google 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 47:217–223

    Article  Google Scholar 

  67. Nakagiri A (2002) Diversity and phylogeny of Halophytophthora (Oomycetes). Abstracts, 7th International Mycological Congress, Oslo. 55 p.19.

  68. Newell SY, Cefalu R, Fell JW (1977) Myzocytium, Haptoglossa and Gonimochaete (fungi) in littoral marine nematodes. Bull Marine Science 27:197–207

    Google Scholar 

  69. Overton SV, Tharp TP, Bland CE (1983) Fine structure of swimming, encysting, and germinating spores of Haliphthoros milfordensis. Can J Bot 61:1165–1177

    Article  Google Scholar 

  70. Padgett DE (1978) Observations on the estuarine distribution of Saprolegniceae. Trans Br Mycol Soc 70:41–143

    Article  Google 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 3:1169–1175

    PubMed  Article  CAS  Google 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 104:1295–1303

    Article  CAS  Google Scholar 

  73. Prakob W, Judelson HS (2007) Gene expression during oosporogenesis in heterothallic and homothallic Phytophthora. Fungal Gen Biol 44:726–739

    Article  CAS  Google 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 63:409–418

    Article  Google 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 58:2557–2574

    Article  Google Scholar 

  76. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous pathogens: gene exchange across eukaryote kingdoms. Curr Biol 16:1857–1864

    PubMed  Article  CAS  Google 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 77:1790–1800

    Article  Google 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 94:834–849

    PubMed  Article  Google Scholar 

  79. Robb EJ, Barron GL (1982) Nature’s ballistic missile. Science 218:1221–1222

    PubMed  Article  CAS  Google Scholar 

  80. Robold A, Hardham AR (2005) During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr Genet 47:307–315

    PubMed  Article  CAS  Google 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 56:1315–1325

    Article  Google Scholar 

  82. Schnepf E, Deichgräber G, Drebes G (1978a) Development and ultrastructure of the marine, parasitic oomycete, Lagenisma coscinodisci Drebes (Lagenidiales). Archiv Microbiol 116:133–139

    Article  Google 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 116:121–132

    Google 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 94:263–280

    Article  Google 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 pp

  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 48:212–221

    Article  CAS  Google 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 112:361–374

    PubMed  Article  CAS  Google 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 159:401–412

    Article  Google 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

    Article  Google Scholar 

  90. Sparrow FK (1960) Aquatic Phycomycetes, 2nd revised edition. University of Michigan Press, Ann Arbor, p 1187

    Google 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 213–222

  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.

  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 450:41–42

    PubMed  Article  CAS  Google 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.

  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.

  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):225–232

    PubMed  Article  CAS  Google 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

    PubMed  Article  Google 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 50:129–140

    Article  Google Scholar 

  100. Tyler BM et al (2006) Phytophthora genome sequences uncover the evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266

    PubMed  Article  CAS  Google 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

    Article  Google 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 110:75–85

    Article  Google 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 450:115–118

    PubMed  Article  CAS  Google Scholar 

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Acknowledgements

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.

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The authors declare that they have no conflict of interest.

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Beakes, G.W., Glockling, S.L. & Sekimoto, S. The evolutionary phylogeny of the oomycete “fungi”. Protoplasma 249, 3–19 (2012). https://doi.org/10.1007/s00709-011-0269-2

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Keywords

  • Apicocomplexa
  • Chromalveolates
  • Eurychasma
  • Haliphthoros
  • Olpidiopsis
  • Oomycetes
  • Pathogenicity
  • Phylogeny
  • Ultrastructure