Distinctive Expansion of Potential Virulence Genes in the Genome of the Oomycete Fish Pathogen Saprolegnia parasitica

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Jiang, Rays H Y ^a   de Bruijn, Irene ^b,g   Haas, Brian J ^a   Belmonte, Rodrigo ^b   Löbach, Lars ^b   Christie, James ^b   van den Ackerveken, Guido ^c   Bottin, Arnaud ^d,e   Bulone, Vincent ^f   Díaz Moreno, Sara M ^f   Dumas, Bernard ^d,e   Fan, Lin ^a   Gaulin, Elodie ^d,e   Govers, Francine ^g,h   Grenville Briggs, Laura J ^b,f   Horner, Neil R ^b   Levin, Joshua Z ^a   Mammella, Marco ⁱ   Meijer, Harold J G ^g   Morris, Paul ^j   Nusbaum, Chad ^a   Oome, Stan ^c   Phillips, Andrew J ^b   van Rooyen, David ^b   Rzeszutek, Elzbieta ^e   Saraiva, Marcia ^b   Secombes, Chris J ^b   Seidl, Michael F ^c,h   Snel, Berend ^c,h   Stassen, Joost H M ^c   Sykes, Sean ^a   Tripathy, Sucheta ^k   van den Berg, Herbert ^b   Vega Arreguin, Julio C ^l   Wawra, Stephan ^b   Young, Sarah K ^a   Zeng, Qiandong ^a   Dieguez Uribeondo, Javier ^m   Russ, Carsten ^a   Tyler, Brett M ^k,n   van West, Pieter ^b   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e Centre National de la Recherche Scientifique   (France)

^f ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^g WAGENINGEN UNIVERSITY   (Netherlands)

^h CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

ⁱ UNIVERSITY MEDITERRANEA OF REGGIO CALABRIA   (Italy)

^j BOWLING GREEN STATE UNIVERSITY   (United States)

^k VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^l UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^m CSIC   (Spain)

ⁿ OREGON STATE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DISINTEGRIN; GALAPTIN; INORGANIC NITROGEN; NITROGEN; PHOSPHOTRANSFERASE; PROTEINASE; SULFUR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FUNGAL GENOME; FUNGAL VIRULENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOME SIZE; HETEROZYGOSITY LOSS; HORIZONTAL GENE TRANSFER; HOST PARASITE INTERACTION; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITISM; PATHOGENESIS; PHYTOPHTHORA; PROTEIN EXPRESSION; RNA SEQUENCE; SAPROLEGNIA; SAPROLEGNIA PARASITICA; SAPROTROPH; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; FISHES; GENE TRANSFER, HORIZONTAL; GENOME; HOST-PARASITE INTERACTIONS; OOMYCETES; PHYLOGENY; PLANTS; SAPROLEGNIA; VIRULENCE;

AMPHIBIA; ANIMALIA; CRUSTACEA; EUKARYOTA; FUNGI; HEXAPODA; OOMYCETES; PHYTOPHTHORA; SAPROLEGNIA PARASITICA; STRAMENOPILES;

EID: 84879653114     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003272     Document Type: Article

References (82)

1. Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ, van West P, (2008) New insights into animal pathogenic oomycetes. TIM 16: 13-19.
2. Van West P, (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20: 99-104.
3. Bruno DW, van West P, GW B (2009) Saprolegnia and other oomycetes. In: Bruno DW, editors. In: Fish Diseases and Disorders, 2nd edition. CABI. pp. 669-720.
4. Denoeud F, Roussel M, Noel B, Wawrzyniak I, Da Silva C, et al. (2011) Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol 12 (3):: R29.
5. Patterson DJ, (1999) The diversity of eukaryotes. American Naturalist 154: S96-S124.
6. Dieguez-Uribeondo J, Garcia MA, Cerenius L, Kozubikova E, Ballesteros I, et al. (2009) Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (Oomycetes). Fungal Genet.Biol 46: 365-376.
7. Tyler BM (2009) Effectors. In: Oomycete Genetics and Genomics. John Wiley & Sons, Inc. pp. 361-385.
8. Van West P, Vleeshouwers VG (2004) The Phytophthora infestans-host interaction. In: Talbot NJ, editor. In: Plant Pathogen Interactions, Annual Plant Reviews. Blackwell Scientific Publishers. pp. 219-242.
9. Tyler BM, (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol Plant Pathol 8: 1-8.
10. Gruenwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S, (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. TIM 20: 131-138.
11. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.
12. 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: 393-398.
13. Lamour K, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, et al. (2012) Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant-Microbe Interact 25: 1350-1360.
14. Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, et al. (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11 (7):: R73.
15. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, et al. (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
16. Links MG, Holub E, Jiang RHY, Sharpe AG, Hegedus D, et al. (2011) De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genomics 12: 503.
17. Jiang RHY, Tyler BM, (2012) Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 50: 295-318.
18. Raffaele S, Kamoun S, (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Rev Microbiol 10: 417-430.
19. Kamoun S, (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44: 41-60.
20. Schornack S, Huitema E, Cano LM, Bozkurt TO, Oliva R, et al. (2009) Ten things to know about oomycete effectors. Mol Plant Pathol 10: 795-803.
21. 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-Sgm 154: 3743-3751.
22. 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: 4874-4879.
23. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, et al. (2010) Ancient class of translocated oomycete effectors targets the host nucleus. PNAS 107: 17421-17426.
24. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115-118.
25. Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. The Plant Cell 20: 1930-1947.
26. Gaulin E, Madoui M-A, Bottin A, Jacquet C, Mathe C, et al. (2008) Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. Plos One 3: e1723.
27. Torto-Alalibo T, Tian MY, Gajendran K, Waugh ME, van West P, et al. (2005) Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiology 5: 46.
28. Van West P, de Bruijn I, Minor KL, Phillips AJ, Robertson EJ, et al. (2010) The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiology 310: 127-137.
29. Krajaejun T, Khositnithikul R, Lerksuthirat T, Lowhnoo T, Rujirawat T, et al. (2011) Expressed sequence tags reveal genetic diversity and putative virulence factors of the pathogenic oomycete Pythium insidiosum. Fungal Biol 115: 683-696.
30. Wawra S, Bain J, Durward E, de Bruijn I, Minor KL, et al. (2012) Host-targeting protein 1 (SpHtp1) from the oomycete Saprolegnia parasitica translocates specifically into fish cells in a tyrosine-O-sulphate-dependent manner. PNAS 109: 2096-2101.
31. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotech 29: 644-U130.
32. Chamnanpunt J, Shan WX, Tyler BM, (2001) High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae. PNAS 98: 14530-14535.
33. MacGregor T, Bhattacharyya M, Tyler B, Bhat R, Schmitthenner AF, et al. (2002) Genetic and physical mapping of Avrla in Phytophthora sojae. Genetics 160: 949-959.
34. Slamovits CH, Keeling PJ, (2009) Evolution of ultrasmall spliceosomal introns in highly reduced nuclear genomes. Mol Biol Evol 26: 1699-1705.
35. Muotri AR, Marchetto MCN, Coufal NG, Gage FH, (2007) The necessary junk: new functions for transposable elements. Human Mol Gen 16: R159-R167.
36. Judelson HS, Ah-Fong AMV, (2010) The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups. BMC Genomics 11: 700.
37. Gaulin E, Drame N, Lafitte C, Torto-Alalibo T, Martinez Y, et al. (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. The Plant Cell 18: 1766-1777.
38. Schneider DJ, Collmer A (2010) Studying plant-pathogen interactions in the genomics era: beyond molecular Koch's Postulates to systems biology. In: VanAlfen NK, Bruening G, Leach JE, editors. Annu. Rev. Phytopathol. Vol 48. pp. 457-479.
39. Guerriero G, Avino M, Zhou Q, Fugelstad J, Clergeot P-H, et al. (2010) Chitin synthases from Saprolegnia are involved in tip growth and represent a potential target for anti-oomycete drugs. PLoS Pathogens 6: e1001070-e1001070.
40. Mélida H, Sandoval-Sierra JV, Diéguez-Uribeondo J, Bulone V, (2013) Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryotic Cell 12: 194-203.
41. Bartnicki-Garcia S, (1968) Cell wall chemistry morphogenesis and taxonomy of fungi. Annu Rev Microbiol 22: 87-108.
42. Bulone V, Chanzy H, Gay L, Girard V, Fevre M, (1992) Characterization of chitin and chitin synthase from the cellulosic cell-wall fungus Saprolegnia monoica. Experimental Mycology 16: 8-21.
43. Badreddine I, Lafitte C, Heux L, Skandalis N, Spanou Z, et al. (2008) Cell wall chitosaccharides are essential components and exposed patterns of the phytopathogenic oomycete Aphanomyces euteiches. Eukaryotic Cell 7: 1980-1993.
44. Gaulin E, Bottin A, Dumas B, (2010) Sterol biosynthesis in oomycete pathogens. Plant signaling & behavior 5: 258-260.
45. Madoui M-A, Bertrand-Michel J, Gaulin E, Dumas B, (2009) Sterol metabolism in the oomycete Aphanomyces euteiches, a legume root pathogen. New Phytologist 183: 291-300.
46. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Research 37: D233-D238.
47. Morris PF, Schlosser LR, Onasch KD, Wittenschlaeger T, Austin R, et al. (2009) Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. Plos One 4: e6133.
48. Seidl MF, Van den Ackerveken G, Govers F, Snel B, (2011) A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization. Plant Physiology 155: 628-644.
49. Gaulin E, Jauneau A, Villalba F, Rickauer M, Esquerre-Tugaye MT, et al. (2002) The CBEL glycoprotein of Phytophthora parasitica var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. Journal of Cell Science 115: 4565-4575.
50. Bjornsdottir B, Fridjonsson OH, Magnusdottir S, Andresdottir V, Hreggvidsson GO, et al. (2009) Characterisation of an extracellular vibriolysin of the fish pathogen Moritella viscosa. Veterinary Microbiology 136: 326-334.
51. Lu Y-J, Schornack S, Spallek T, Geldner N, Chory J, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cellular Microbiology 14: 682-697.
52. Huitema E, Vleeshouwers V, Cakir C, Kamoun S, Govers F, (2005) Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INN, INF2A, and INF2B of Phytophthora infestans. Molecular Plant-Microbe Interactions 18: 183-193.
53. Jiang RHY, Tyler BM, Whisson SC, Hardham AR, Govers F, (2006) Ancient origin of elicitin gene clusters in Phytophthora genomes. Molecular Biology and Evolution 23: 338-351.
54. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, et al. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540-1543.
55. Vernikos GS, Parkhill J, (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196-2203.
56. Beakes GW, Glockling SL, Sekimoto S, (2012) The evolutionary phylogeny of the oomycete "fungi". Protoplasma 249: 3-19.
57. Küpper FC, Maier I, Müller G, Loiseaux-De Goer S, Guillou L, (2006) Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Coh. Cryptogamie, Algologie 27: 165-184.
58. Bateman A, Rawlings ND, (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends in Biochemical Sciences 28: 234-237.
59. Hunt S, Green J, Artymiuk PJ (2010) Hemolysin E (HlyE, ClyA, SheA) and related toxins. In: Anderluh G, Lakey J, editors. Proteins: Membrane Binding and Pore Formation. pp. 116-126.
60. Ozeki Y, Matsui T, Suzuki M, Titani K, (1991) Amino acid sequence and molecular characterization of a D-galactoside-specific lectin purified from sea-urchin (Anthocidaris crassipina) eggs. Biochemistry 30: 2391-2394.
61. Ozeki Y, Yokota Y, Kato KH, Titani K, Matsui T, (1995) Developmental expression of D-galactoside-binding lectin in sea urchin (Anthocidaris crassipina) eggs. Experimental Cell Research 216: 318-324.
62. Ogawa T, Watanabe M, Naganuma T, Muramoto K, (2011) Diversified carbohydrate-binding lectins from marine resources. Journal of amino acids 2011: 838914-838914.
63. McLane M, Sanchez E, Wong A, Paquette-Straub C, Perez JC, (2004) Disintegrins. Curr Drug Targets Cardiovasc Haematol Disord 4: 327-355.
64. Ebstrup T, Saalbach G, Egsgaard H, (2005) A proteomics study of in vitro cyst germination and appressoria formation in Phytophthora infestans. Proteomics 5: 2839-2848.
65. Shan WX, Marshall JS, Hardham AR, (2004) Gene expression in germinated cysts of Phytophthora nicotianae. Molecular Plant Pathology 5: 317-330.
66. Torto-Alalibo TA, Tripathy S, Smith BM, Arredondo FD, Zhou L, et al. (2007) Expressed sequence tags from Phytophthora sojae reveal genes specific to development and infection. Molecular Plant-Microbe Interactions 20: 781-793.
67. Ye W, Wang X, Tao K, Lu Y, Dai T, et al. (2011) Digital gene expression profiling of the Phytophthora sojae transcriptome. Molecular Plant-Microbe Interactions 24: 1530-1539.
68. Rosenblum EB, Stajich JE, Maddox N, Eisen MB, (2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 105: 17034-17039.
69. McDowell JM, (2011) Genomes of obligate plant pathogens reveal adaptations for obligate parasitism. Proceedings of the National Academy of Sciences of the United States of America 108: 8921-8922.
70. Stueland S, Hatai K, Skaar I, (2005) Morphological and physiological characteristics of Saprolegnia spp. strains pathogenic to Atlantic salmon, Salmo salar L. Journal of Fish Diseases 28: 445-453.
71. Wolf K, Quimby MC, (1962) Established eurythermic line of fish cell in vitro. Science 135: 1065-1066.
72. Lennon NJ, Lintner RE, Anderson S, Alvarez P, Barry A, et al. (2010) A scalable, fully automated process for construction of sequence-ready barcoded libraries for 454. Genome Biology 11: R15.
73. Fisher S, Barry A, Abreu J, Minie B, Nolan J, et al. (2011) A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biology 12: R1.
74. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nature Methods 7: 709-U767.
75. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
76. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297-1303.
77. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research 31: 5654-5666.
78. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332: 930-936.
79. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
80. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate- a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289-300.
81. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M, (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research 32: D277-D280.
82. Hudson L, Hay F (1980) Practical Immunology. London, UK: Blackwell Scientific Publications. pp. 1-9, 113-137, 227-229.