A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization

Plant Physiology

Volumn 155, Issue 2, 2011, Pages 628-644

  Seidl, Michael F ^a,b,c   van den Ackerveken, Guido ^a,b   Govers, Francine ^b,c   Snel, Berend ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMALVEOLATA; EUKARYOTA; FUNGI; OOMYCETES;

EID: 79551698024     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.167841     Document Type: Article

References (74)

1. Agrios GN (2005) Plant Pathology, Ed 5. Academic Press, New York
2. Amann M, Wanner G, Zenk MH (1986) Intracellular compartmentation of two enzymes of berberine biosynthesis in plant cell cultures. Planta 167: 310-320
3. Aravind L, Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22: 458-459
4. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdomlevel phylogeny of eukaryotes based on combined protein data. Science 290: 972-977
5. Bashton M, Chothia C (2007) The generation of new protein functions by the combination of domains. Structure 15: 85-99
6. Basu MK, Carmel L, Rogozin IB, Koonin EV (2008) Evolution of protein domain promiscuity in eukaryotes. Genome Res 18: 449-461
7. Baurain D, Brinkmann H, Petersen J, Rodríguez-Ezpeleta N, Stechmann A, Demoulin V, Roger AJ, Burger G, Lang BF, Philippe H (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27: 1698-1709
8. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: Signal P 3.0. J Mol Biol 340: 783-795
9. Blair JE, Coffey MD, Park SY, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45: 266-277
10. Buljan M, Frankish A, Bateman A (2010) Quantifying the mechanisms of domain gain in animal proteins. Genome Biol 11: R74
11. Cosentino Lagomarsino M, Sellerio AL, Heijning PD, Bassetti B (2009) Universal features in the genome-level evolution of protein domains. Genome Biol 10: R12
12. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, et al (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986
13. Doolittle RF (1995) The multiplicity of domains in proteins. Annu Rev Biochem 64: 287-314
14. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14: 755-763
15. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
16. Erwin DC, Ribeiro OK (1996) Phytophthora Diseases Worldwide. American Phytopathological Society, St. Paul
17. Facchini PJ, Penzes C, Johnson AG, Bull D (1996) Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol 112: 1669-1677
18. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, et al (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-D288
19. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
20. Gijzen M, Nürnberger T (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67: 1800-1807
21. Govers F, Gijzen M (2006) Phytophthora genomics: the plant destroyers' genome decoded. Mol Plant Microbe Interact 19: 1295-1301
22. Groves MR, Taylor MA, Scott M, Cummings NJ, Pickersgill RW, Jenkins JA (1996) The prosequence of procaricain forms an alpha-helical domain that prevents access to the substrate-binding cleft. Structure 4: 1193- 1203
23. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398
24. He SY, Collmer A (1990) Molecular cloning, nucleotide sequence, and marker exchange mutagenesis of the exo-poly-alpha-D-galacturonosidase- encoding pehX gene of Erwinia chrysanthemi EC16. J Bacteriol 172: 4988-4995
25. Inohara N, Nuñez G (2002) ML: a conserved domain involved in innate immunity and lipid metabolism. Trends Biochem Sci 27: 219-221
26. Itoh T, Hashimoto W, Mikami B, Murata K (2006) Substrate recognition by unsaturated glucuronyl hydrolase from Bacillus sp. GL1. Biochem Biophys Res Commun 344: 253-262
27. Iyer LM, Anantharaman V, Wolf MY, Aravind L (2008) Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol 38: 1-31
28. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, et al (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443: 818-822
29. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066
30. Kawamukai M, Utsumi R, Takeda K, Higashi A, Matsuda H, Choi YL, Komano T (1991) Nucleotide sequence and characterization of the sfs1 gene: sfs1 is involved in CRP*-dependent mal gene expression in Escherichia coli. J Bacteriol 173: 2644-2648
31. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605-618
32. Klis FM, Sosinska GJ, de Groot PW, Brul S (2009) Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEM Yeast Res 9: 1013-1028
33. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580
34. Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28: 118-121
35. Kutchan TM, Dittrich H (1995) Characterization and mechanism of the berberine bridge enzyme, a covalently flavinylated oxidase of benzophenanthridine alkaloid biosynthesis in plants. J Biol Chem 270: 24475- 24481
36. Latijnhouwers M, de Wit PJGM, Govers F (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol 11: 462-469
37. Lévesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, et al (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11: R73
38. Liu Z, Bos JI, Armstrong M, Whisson SC, da Cunha L, Torto-Alalibo T, Win J, Avrova AO, Wright F, Birch PR, et al (2005) Patterns of diversifying selection in the phytotoxin-like scr74 gene family of Phytophthora infestans. Mol Biol Evol 22: 659-672
39. Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO, Eisenberg D (1999) Detecting protein function and protein-protein interactions from genome sequences. Science 285: 751-753
40. Marsh JA, Teichmann SA (2010) How do proteins gain new domains? Genome Biol 11: 126
41. Martens C, Vandepoele K, Van de Peer Y (2008) Whole-genome analysis reveals molecular innovations and evolutionary transitions in chromalveolate species. Proc Natl Acad Sci USA 105: 3427-3432
42. Martinez SE, Beavo JA, Hol WGJ (2002) GAF domains: two-billionyear- old molecular switches that bind cyclic nucleotides. Mol Interv 2: 317-323
43. McLeod A, Smart CD, Fry WE (2003) Characterization of 1,3-beta-glucanase and 1,3;1,4-beta-glucanase genes from Phytophthora infestans. Fungal Genet Biol 38: 250-263
44. Meijer HJG, Govers F (2006) Genomewide analysis of phospholipid signaling genes in Phytophthora spp.: novelties and a missing link. Mol Plant Microbe Interact 19: 1337-1347
45. Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7: 357-366
46. Morris PF, Schlosser LR, Onasch KD, Wittenschlaeger T, Austin R, Provart N (2009) Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. PLoS ONE 4: e6133
47. Moy P, Qutob D, Chapman BP, Atkinson I, Gijzen M (2004) Patterns of gene expression upon infection of soybean plants by Phytophthora sojae. Mol Plant Microbe Interact 17: 1051-1062
48. Okamura K, Hagiwara-Takeuchi Y, Li T, Vu TH, Hirai M, Hattori M, Sakaki Y, Hoffman AR, Ito T (2000) Comparative genome analysis of the mouse imprinted gene impact and its nonimprinted human homolog IMPACT: toward the structural basis for species-specific imprinting. Genome Res 10: 1878-1889
49. Oliveros JC (2007) VENNY: An Interactive Tool for Comparing Lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html (October 7, 2010)
50. Orengo CA, Michie AD, Jones S, Jones DT, Swindells MB, Thornton JM (1997) CATH: a hierarchic classification of protein domain structures. Structure 5: 1093-1108
51. Orsomando G, Lorenzi M, Raffaelli N, Dalla Rizza M, Mezzetti B, Ruggieri S (2001) Phytotoxic protein PcF, purification, characterization, and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum. J Biol Chem 276: 21578-21584
52. Park F, Gajiwala K, Eroshkina G, Furlong E, He D, Batiyenko Y, Romero R, Christopher J, Badger J, Hendle J, et al (2004) Crystal structure of YIGZ, a conserved hypothetical protein from Escherichia coli K12 with a novel fold. Proteins 55: 775-777
53. Park J, Lappe M, Teichmann SA (2001) Mapping protein family interactions: intramolecular and intermolecular protein family interaction repertoires in the PDB and yeast. J Mol Biol 307: 929-938
54. Pathak D, Ashley G, Ollis D (1991) Thiol protease-like active site found in the enzyme dienelactone hydrolase: localization using biochemical, genetic, and structural tools. Proteins 9: 267-279
55. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 96: 4285-4288
56. Raffaele S, Win J, Cano L, Kamoun S (2010) Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genomics 11: 637
57. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
58. Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113-1118
59. Richards TA, Talbot NJ (2007) Plant parasitic oomycetes such as Phytophthora species contain genes derived from three eukaryotic lineages. Plant Signal Behav 2: 112-114
60. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of nucleotide-binding protein. Nature 250: 194-199
61. Ruttkowski E, Labitzke R, Khanh NQ, Löffler F, Gottschalk M, Jany KD (1990) Cloning and DNA sequence analysis of a polygalacturonase cDNA from Aspergillus niger RH5344. Biochim Biophys Acta 1087: 104-106
62. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193
63. Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev 3: 1745-1757
64. Simpson AGB, Roger AJ (2004) The real 'kingdoms' of eukaryotes. Curr Biol 14: R693-R696
65. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690
66. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445
67. Terashima H, Fukuchi S, Nakai K, Arisawa M, Hamada K, Yabuki N, Kitada K (2002) Sequence-based approach for identification of cell wall proteins in Saccharomyces cerevisiae. Curr Genet 40: 311-316
68. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266
69. Vogel C, Bashton M, Kerrison ND, Chothia C, Teichmann SA (2004) Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol 14: 208-216
70. Vogel C, Teichmann SA, Pereira-Leal J (2005) The relationship between domain duplication and recombination. J Mol Biol 346: 355-365
71. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, et al (2008) TMEM16A confers receptor-activated calciumdependent chloride conductance. Nature 455: 1210-1215
72. Yin QY, de Groot PW, Dekker HL, de Jong L, Klis FM, de Koster CG (2005) Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J Biol Chem 280: 20894-20901
73. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99: 15507-15512
74. Zoraghi R, Corbin JD, Francis SH (2004) Properties and functions of GAF domains in cyclic nucleotide phosphodiesterases and other proteins. Mol Pharmacol 65: 267-278