The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Judelson, Howard S ^a   Ah Fong, Audrey M V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; MESSENGER RNA; PROTEIN KINASE; PROTEIN TYROSINE KINASE;

ALGAL GENETICS; APICOMPLEXA; ARTICLE; BIOINFORMATICS; CLADISTICS; CROSSING OVER; DIATOM; ENZYME ACTIVITY; ENZYME ANALYSIS; FUNGUS HYPHAE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; GENOME ANALYSIS; HYALOPERONOSPORA ARABIDOPSIDIS; LIFE CYCLE; MOLECULAR EVOLUTION; NONHUMAN; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; PHYTOPHTHORA RAMORUM; PHYTOPHTHORA SOJAE; PLANT TAXONOMY; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SPORANGIUM; TRANSCRIPTION REGULATION; ZOOSPORE; AMINO ACID SEQUENCE; BIOCATALYSIS; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

APICOMPLEXA; BACILLARIOPHYTA; CILIOPHORA; EUKARYOTA; HYALOPERONOSPORA; METAZOA; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; PHYTOPHTHORA RAMORUM; PHYTOPHTHORA SOJAE;

AMINO ACID SEQUENCE; BIOCATALYSIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOME; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OOMYCETES; PHYLOGENY; PHYTOPHTHORA INFESTANS; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY;

EID: 78649784580     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-700     Document Type: Article

References (59)

1. Hanks SK, Hunter T. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J 1995, 9:576-596.
2. LaRonde-LeBlanc N, Wlodawer A. The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. Biochim Biophys Acta 2005, 1754:14-24.
3. Wuichet K, Cantwell BJ, Zhulin IB. Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 2010, 13:219-225. 10.1016/j.mib.2009.12.011, 20133179.
4. Becker W, Joost HG. Structural and functional characteristics of Dyrk, a novel subfamily of protein kinases with dual specificity. Prog Nucleic Acid Res Mol Biol 1999, 62:1-17. 10.1016/S0079-6603(08)60503-6, 9932450.
5. Deshmukh K, Anamika K, Srinivasan N. Evolution of domain combinations in protein kinases and its implications for functional diversity. Prog Biophys Mol Biol 2010, 102:1-15. 10.1016/j.pbiomolbio.2009.12.009, 20026163.
6. Champion A, Kreis M, Mockaitis K, Picaud A, Henry Y. Arabidopsis kinome: after the casting. Funct Integr Genomics 2004, 4:163-187. 10.1007/s10142-003-0096-4, 14740254.
7. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934. 10.1126/science.1075762, 12471243.
8. Manning G, Plowman GD, Hunter T, Sudarsanam S. Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 2002, 27:514-520. 10.1016/S0968-0004(02)02179-5, 12368087.
9. Manning G, Young SL, Miller WT, Zhai Y. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc Natl Acad Sci USA 2008, 105:9674-9679. 10.1073/pnas.0801314105, 2453073, 18621719.
10. Goldberg JM, Manning G, Liu A, Fey P, Pilcher KE, Xu Y, Smith JL. The Dictyostelium kinome--analysis of the protein kinases from a simple model organism. PLoS Genet 2006, 2:e38. 10.1371/journal.pgen.0020038, 1420674, 16596165.
11. Bemm F, Schwarz R, Forster F, Schultz J. A kinome of 2600 in the ciliate Paramecium tetraurelia. FEBS Lett 2009, 583:3589-3592. 10.1016/j.febslet.2009.10.029, 19840790.
12. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 2003, 132:666-680. 10.1104/pp.102.011999, 167006, 12805596.
13. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005, 52:399-451. 10.1111/j.1550-7408.2005.00053.x, 16248873.
14. Simpson AG, Roger AJ. The real 'kingdoms' of eukaryotes. Curr Biol 2004, 14:R693-696. 10.1016/j.cub.2004.08.038, 15341755.
15. Fry W. Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 2008, 9:385-402. 10.1111/j.1364-3703.2007.00465.x, 18705878.
16. Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nature Microbiol Rev 2005, 3:47-58.
17. Judelson HS, Roberts S. Novel protein kinase induced during sporangial cleavage in the oomycete Phytophthora infestans. Eukaryot Cell 2002, 1:687-695. 10.1128/EC.1.5.687-695.2002, 126747, 12455688.
18. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AM, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JI, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461:393-398. 10.1038/nature08358, 19741609.
19. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CM, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee MK, McDonald WH, Medina M, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006, 313:1261-1266. 10.1126/science.1128796, 16946064.
20. Montsant A, et al. Identification and comparative genomic analysis of signaling and regulatory components in the diatom Thalassiosira pseudonana. J Phycol 2007, 43:585-604.
21. Boudeau J, Miranda-Saavedra D, Barton GJ, Alessi DR. Emerging roles of pseudokinases. Trends Cell Biol 2006, 16:443-452. 10.1016/j.tcb.2006.07.003, 16879967.
22. Parsons M, Worthey EA, Ward PN, Mottram JC. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 2005, 6:127. 10.1186/1471-2164-6-127, 1266030, 16164760.
23. Morris PF, Schlosser LR, Onasch KD, Wittenschlaeger T, Austin R, Provart N. Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. PLoS One 2009, 4:e6133. 10.1371/journal.pone.0006133, 2705460, 19582169.
24. Bogre L, Okresz L, Henriques R, Anthony RG. Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 2003, 8:424-431. 10.1016/S1360-1385(03)00188-2, 13678909.
25. Meijer HJ, Govers F. Genomewide analysis of phospholipid signaling genes in Phytophthora spp.: novelties and a missing link. Mol Plant Microbe Interact 2006, 19:1337-1347. 10.1094/MPMI-19-1337, 17153918.
26. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 2000, 290:972-977. 10.1126/science.290.5493.972, 11062127.
27. Harmon AC, Gribskov M, Gubrium E, Harper JF. The CDPK superfamily of protein kinases. New Phytol 2001, 151:175-183.
28. Deacon JW, Donaldson SP. Molecular recognition in the homing responses of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycol Res 1993, 97:1153-1171.
29. Cheng S-H, Willmann MR, Chen H-C, Sheen J. Calcium signaling through protein kinases The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 2002, 129:469-485. 10.1104/pp.005645, 1540234, 12068094.
30. Srinivasan N, Krupa A. A genomic perspective of protein kinases in Plasmodium falciparum. Proteins 2005, 58:180-189.
31. Harmon AC, Gribskov M, Harper JF. CDPKs: A kinase for every Ca2+ signal?. Trends Plant Sci 2000, 5:154-159. 10.1016/S1360-1385(00)01577-6, 10740296.
32. Gaffin SL. Simplified calcium transport and storage pathways. J Thermal Biol 1999, 24:251-264.
33. Malumbres M, Harlow E, Hunt T, Hunter T, Lahti JM, Manning G, Morgan DO, Tsai LH, Wolgemuth DJ. Cyclin-dependent kinases: a family portrait. Nat Cell Biol 2009, 11:1275-1276. 10.1038/ncb1109-1275, 2914104, 19884882.
34. Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 2004, 135:1084-1099. 10.1104/pp.104.040436, 514142, 15208425.
35. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912. 10.1126/science.1072682, 12471242.
36. Nakagami H, Pitzschke A, Hirt H. Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 2005, 10:339-346. 10.1016/j.tplants.2005.05.009, 15953753.
37. Ward P, Equinet L, Packer J, Doerig C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 2004, 5:79. 10.1186/1471-2164-5-79, 526369, 15479470.
38. Champion A, Picaud A, Henry Y. Reassessing the MAP3K and MAP4K relationships. Trends Plant Sci 2004, 9:123-129. 10.1016/j.tplants.2004.01.005, 15003235.
39. Meylan E, Tschopp J. IRAK2 takes its place in TLR signaling. Nat Immunol 2008, 9:581-582. 10.1038/ni0608-581, 18490904.
40. Shiu SH, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 2001, 98:10763-10768. 10.1073/pnas.181141598, 58549, 11526204.
41. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456:239-244. 10.1038/nature07410, 18923393.
42. Shiu SH, Li WH. Origins, lineage-specific expansions, and multiple losses of tyrosine kinases in eukaryotes. Mol Biol Evol 2004, 21:828-840. 10.1093/molbev/msh077, 14963097.
43. Miranda-Saavedra D, Barton GJ. Classification and functional annotation of eukaryotic protein kinases. Proteins 2007, 68:893-914. 10.1002/prot.21444, 17557329.
44. Martin DM, Miranda-Saavedra D, Barton GJ. Kinomer v. 1.0: a database of systematically classified eukaryotic protein kinases. Nucleic Acids Res 2009, 37:D244-250. 10.1093/nar/gkn834, 2686601, 18974176.
45. Rudrabhatla P, Reddy MM, Rajasekharan R. Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 2006, 60:293-319. 10.1007/s11103-005-4109-7, 16429265.
46. Ah Fong A, Judelson HS. Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Molec Microbiol 2003, 50:487-494.
47. Judelson HS, Ah-Fong AM, Aux G, Avrova AO, Bruce C, Cakir C, da Cunha L, Grenville-Briggs L, Latijnhouwers M, Ligterink W, Meijer HJ, Roberts S, Thurber CS, Whisson SC, Birch PR, Govers F, Kamoun S, van West P, Windass J. Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol Plant Microbe Interact 2008, 21:433-447. 10.1094/MPMI-21-4-0433, 18321189.
48. Bradley BA, Quarmby LM. A NIMA-related kinase, Cnk2p, regulates both flagellar length and cell size in Chlamydomonas. J Cell Sci 2005, 118:3317-3326. 10.1242/jcs.02455, 16030138.
49. Clark MC, Melanson DL, Page OT. Purine metabolism and differential inhibition of spore germination in Phytophthora infestans. Can J Microbiol 1978, 24:1032-1038. 10.1139/m78-171, 709431.
50. Riethmueller A, Voglmayr H, Goeker M, Weiss M, Oberwinkler F. Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia 2002, 94:834-849.
51. Slusarenko AJ, Schlaich NL. Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Molec Plant Pathol 2003, 4:159-170.
52. Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, Ammar R, Staskawicz BJ, Kamoun S. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 2007, 19:2349-2369. 10.1105/tpc.107.051037, 2002621, 17675403.
53. Smythe E, Ayscough KR. The Ark1/Prk1 family of protein kinases. Regulators of endocytosis and the actin skeleton. EMBO Rep 2003, 4:246-251. 10.1038/sj.embor.embor776, 1315904, 12634840.
54. Alam I, Hubbard SJ, Oliver SG, Rattray M. A kingdom-specific protein domain HMM library for improved annotation of fungal genomes. BMC Genomics 2007, 8:97. 10.1186/1471-2164-8-97, 1854895, 17425790.
55. Blanco FA, Judelson HS. A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Molec Microbiol 2005, 56:638-648.
56. Cohen P. Protein kinases-the major drug targets of the twenty-first century?. Nat Rev Drug Discov 2002, 1:309-315. 10.1038/nrd773, 12120282.
57. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224. 10.1093/molbev/msp259, 19854763.
58. Garrigos M, Deschamps S, Viel A, Lund S, Champeil P, Moller JV, le Maire M. Detection of Ca2+-binding proteins by electrophoretic migration in the presence of Ca2+ combined with 45Ca2+ overlay of protein blots. Anal Biochem 1991, 194:82-88. 10.1016/0003-2697(91)90154-L, 1831012.
59. Dardick C, Chen J, Richter T, Ouyang S, Ronald P. The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol 2007, 143:579-586. 10.1104/pp.106.087270, 1803753, 17172291.