Phylogenomic analyses of malaria parasites and evolution of their exported proteins

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Pick, Christian ^a   Ebersberger, Ingo ^b   Spielmann, Tobias ^c   Bruchhaus, Iris ^c   Burmester, Thorsten ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; GENOME; GENOMICS; MALARIA; PATHOGENICITY; PHYLOGENETICS; PHYLOGENY; PRIMATE; PROTEIN; PROTOZOAN;

AVES; HOMINIDAE; PLASMODIUM FALCIPARUM;

BACTERIAL TOXIN; PROTOZOAL PROTEIN;

ARTICLE; CLASSIFICATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MALARIA; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; PLASMODIUM; PROTEIN MOTIF; PROTEIN TRANSPORT; SECRETORY PATHWAY; SEQUENCE ALIGNMENT;

AMINO ACID MOTIFS; BACTERIAL TOXINS; EVOLUTION, MOLECULAR; HUMANS; MALARIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMODIUM; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SECRETORY PATHWAY; SEQUENCE ALIGNMENT;

EID: 79958767122     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-167     Document Type: Article

References (71)

1. World malaria report 2009. World Health Organization, Geneva 2009
2. Historical review. MF Boyd, In Malariology Philadelphia: W.B. Saunders, Boyd, MF, 1949 2 3 25
3. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. AA Escalante FJ Ayala, Proc Natl Acad Sci USA 1994 9 11373 11377 (Pubitemid 24356346)
4. A new malaria agent in African hominids. B Ollomo P Durand F Prugnolle E Douzery C Arnathau D Nkoghe E Leroy F Renaud, PLoS Pathog 2009 5 1000446 10.1371/journal.ppat.1000446 19478877
5. The origin of malignant malaria. SM Rich FH Leendertz G Xu M LeBreton CF Djoko MN Aminake EE Takang JL Diffo BL Pike BM Rosenthal P Formenty C Boesch FJ Ayala ND Wolfe, Proc Natl Acad Sci USA 2009 106 14902 14907 10.1073/pnas. 0907740106 19666593
6. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. L Duval M Fourment E Nerrienet D Rousset SA Sadeuh SM Goodman NV Andriaholinirina M Randrianarivelojosia RE Paul V Robert FJ Ayala F Ariey, Proc Natl Acad Sci USA 2010 107 10561 10566 10.1073/pnas.1005435107 20498054
7. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. S Krief AA Escalante MA Pacheco L Mugisha C André M Halbwax A Fischer JM Krief JM Kasenene M Crandfield OE Cornejo JM Chavatte C Lin F Letourneur AC Grüner TF McCutchan L Rénia G Snounou, PLoS Pathog 2010 6 1000765 10.1371/journal.ppat.1000765 20169187
8. Origin of the human malaria parasite Plasmodium falciparum in gorillas. W Liu Y Li GH Learn RS Rudicell JD Robertson BF Keele JB Ndjango CM Sanz DB Morgan S Locatelli MK Gonder PJ Kranzusch PD Walsh E Delaporte E Mpoudi-Ngole AV Georgiev MN Muller GM Shaw M Peeters PM Sharp JC Rayner BH Hahn, Nature 2010 467 420 425 10.1038/nature09442 20864995
9. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. F Prugnolle P Durand C Neel B Ollomo FJ Ayala C Arnathau L Etienne E Mpoudi-Ngole D Nkoghe E Leroy E Delaporte M Peeters F Renaud, Proc Natl Acad Sci USA 2010 107 1458 1463 10.1073/pnas.0914440107 20133889
10. Bayesian analysis of new and old malaria parasite DNA sequence data demonstrates the need for more phylogenetic signal to clarify the descent of Plasmodium falciparum. SC Hagner B Misof WA Maier H Kampen, Parasitol Res 2007 101 493 503 10.1007/s00436-007-0499-6 17393186 (Pubitemid 47101405)
11. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. AG Maier M Rug MT O'Neill M Brown S Chakravorty T Szestak J Chesson Y Wu K Hughes RL Coppel C Newbold JG Beeson A Craig BS Crabb AF Cowman, Cell 2008 134 48 61 10.1016/j.cell.2008.04.051 18614010 (Pubitemid 351905737)
12. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. DI Baruch BL Pasloske HB Singh X Bi XC Ma M Feldman TF Taraschi RJ Howard, Cell 1995 82 77 87 10.1016/0092-8674(95)90054-3 7541722
13. Targeting malaria virulence and remodeling proteins to the host erythrocyte. M Marti RT Good M Rug E Knuepfer AF Cowman, Science 2004 306 1930 1933 10.1126/science.1102452 15591202 (Pubitemid 39627856)
14. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. NL Hiller S Bhattacharjee C van Ooij K Liolios T Harrison C Lopez-Estrão K Haldar, Science 2004 306 1934 1937 10.1126/science.1102737 15591203 (Pubitemid 39627857)
15. N-terminal processing of proteins exported by malaria parasites. HH Chang AM Falick PM Carlton JW Sedat JL DeRisi MA Marletta, Mol Biochem Parasitol 2008 160 107 115 10.1016/j.molbiopara.2008.04.011 18534695
16. An aspartyl protease directs malaria effector proteins to the host cell. JA Boddey AN Hodder S Günther PR Gilson H Patsiouras EA Kapp JA Pearce TF de Koning-Ward RJ Simpson BS Crabb AF Cowman, Nature 2010 463 627 631 10.1038/nature08728 20130643
17. Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. I Russo S Babbitt V Muralidharan T Butler A Oksman DE Goldberg, Nature 2010 463 632 636 10.1038/nature08726 20130644
18. A newly discovered protein export machine in malaria parasites. TF de Koning-Ward PR Gilson JA Boddey M Rug BJ Smith AT Papenfuss PR Sanders RJ Lundie AG Maier AF Cowman BS Crabb, Nature 2009 459 945 949 10.1038/nature08104 19536257
19. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. TJ Sargeant M Marti E Caler JM Carlton K Simpson TP Speed AF Cowman, Genome Biol 2006 7 12 10.1186/gb-2006-7-2-r12 16507167
20. The malaria secretome: from algorithms to essential function in blood stage infection. C van Ooij P Tamez S Bhattacharjee NL Hiller T Harrison K Liolios T Kooij J Ramesar B Balu J Adams AP Waters CJ Janse K Haldar, PLoS Pathog 2008 4 1000084 10.1371/journal.ppat.1000084 18551176
21. Moving in and renovating: exporting proteins from Plasmodium into host erythrocytes. DE Goldberg AF Cowman, Nat Rev Microbiol 2010 8 617 621 10.1038/nrmicro2420 20706280
22. A Plasmodium falciparum host-targeting motif functions in export during blood stage infection of the rodent malarial parasite Plasmodium berghei. JJ MacKenzie ND Gámez S Bhattacharjee S Mann K Haldar, PLoS One 2008 3 2405 10.1371/journal.pone.0002405 18545649
23. Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways? T Spielmann TW Gilberger, Trends Parasitol 2010 26 6 10 10.1016/j.pt.2009.10.001 19879191
24. Genome sequence of the human malaria parasite Plasmodium falciparum. MJ Gardner N Hall E Fung O White M Berriman RW Hyman JM Carlton A Pain KE Nelson S Bowman IT Paulsen K James JA Eisen K Rutherford SL Salzberg A Craig S Kyes MS Chan V Nene SJ Shallom B Suh J Peterson S Angiuoli M Pertea J Allen J Selengut D Haft MW Mather AB Vaidya DM Martin AH Fairlamb MJ Fraunholz DS Roos SA Ralph GI McFadden LM Cummings GM Subramanian C Mungall JC Venter DJ Carucci SL Hoffman C Newbold RW Davis CM Fraser B Barrell, Nature 2002 419 498 511 10.1038/nature01097 12368864
25. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. JM Carlton SV Angiuoli BB Suh TW Kooij M Pertea JC Silva MD Ermolaeva JE Allen JD Selengut HL Koo JD Peterson M Pop DS Kosack MF Shumway SL Bidwell SJ Shallom SE van Aken SB Riedmuller TV Feldblyum JK Cho J Quackenbush M Sedegah A Shoaibi LM Cummings L Florens JR Yates JD Raine RE Sinden MA Harris DA Cunningham PR Preiser LW Bergman AB Vaidya LH van Lin CJ Janse AP Waters HO Smith OR White SL Salzberg JC Venter CM Fraser SL Hoffman MJ Gardner DJ Carucci, Nature 2002 419 512 519 10.1038/nature01099 12368865
26. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. N Hall M Karras JD Raine JM Carlton TW Kooij M Berriman L Florens CS Janssen A Pain GK Christophides K James K Rutherford B Harris D Harris C Churcher MA Quail D Ormond J Doggett HE Trueman J Mendoza SL Bidwell MA Rajandream DJ Carucci JR Yates FC Kafatos CJ Janse B Barrell CM Turner AP Waters RE Sinden, Science 2005 307 82 86 10.1126/science.1103717 15637271 (Pubitemid 40093481)
27. The genome of the simian and human malaria parasite Plasmodium knowlesi. A Pain U Böhme AE Berry K Mungall RD Finn AP Jackson T Mourier J Mistry EM Pasini MA Aslett S Balasubrammaniam K Borgwardt K Brooks C Carret TJ Carver I Cherevach T Chillingworth TG Clark MR Galinski N Hall D Harper D Harris H Hauser A Ivens CS Janssen T Keane N Larke S Lapp M Marti S Moule IM Meyer D Ormond N Peters M Sanders S Sanders TJ Sargeant M Simmonds F Smith R Squares S Thurston AR Tivey D Walker B White E Zuiderwijk C Churcher MA Quail AF Cowman CM Turner MA Rajandream CH Kocken AW Thomas CI Newbold BG Barrell M Berriman, Nature 2008 455 799 803 10.1038/nature07306 18843368
28. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. JM Carlton JH Adams JC Silva SL Bidwell H Lorenzi E Caler J Crabtree SV Angiuoli EF Merino P Amedeo Q Cheng RM Coulson BS Crabb HA Del Portillo K Essien TV Feldblyum C Fernandez-Becerra PR Gilson AH Gueye X Guo S Kang'a TW Kooij M Korsinczky EV Meyer V Nene I Paulsen O White SA Ralph Q Ren TJ Sargeant SL Salzberg CJ Stoeckert SA Sullivan MM Yamamoto SL Hoffman JR Wortman MJ Gardner MR Galinski JW Barnwell CM Fraser-Liggett, Nature 2008 455 757 763 10.1038/nature07327 18843361
29. PlasmoDB: a functional genomic database for malaria parasites. C Aurrecoechea J Brestelli BP Brunk S Fischer B Gajria X Gao A Gingle G Grant OS Harb M Heiges F Innamorato J Iodice JC Kissinger ET Kraemer W Li JA Miller V Nayak C Pennington DF Pinney DS Roos C Ross G Srinivasamoorthy CJ Stoeckert Jr R Thibodeau C Treatman H Wang, Nucleic Acids Res 2009 37 539 543 10.1093/nar/gkn814 18957442
30. ToxoDB: an integrated Toxoplasma gondii database resource. B Gajria A Bahl J Brestelli J Dommer S Fischer X Gao M Heiges J Iodice JC Kissinger AJ Mackey DF Pinney DS Roos CJ Stoeckert Jr H Wang BP Brunk, Nucleic Acids Res 2008 36 553 556 18003657
31. Integr8 and Genome Reviews: integrated views of complete genomes and proteomes. P Kersey L Bower L Morris A Horne R Petryszak C Kanz A Kanapin U Das K Michoud I Phan A Gattiker T Kulikova N Faruque K Duggan P Mclaren B Reimholz L Duret S Penel I Reuter R Apweiler, Nucleic Acids Res 2005 33 297 302 15608201
32. CryptoDB: a Cryptosporidium bioinformatics resource update. M Heiges H Wang E Robinson C Aurrecoechea X Gao N Kaluskar P Rhodes S Wang CZ He Y Su J Miller E Kraemer JC Kissinger, Nucleic Acids Res 2006 34 419 422 10.1093/nar/gkj078 16381902
33. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. A Pain H Renauld M Berriman L Murphy CA Yeats W Weir A Kerhornou M Aslett R Bishop C Bouchier M Cochet RM Coulson A Cronin EP de Villiers A Fraser N Fosker M Gardner A Goble S Griffiths-Jones DE Harris F Katzer N Larke A Lord P Maser S McKellar P Mooney F Morton V Nene S O'Neil C Price MA Quail E Rabbinowitsch ND Rawlings S Rutter D Saunders K Seeger T Shah R Squares S Squares A Tivey AR Walker J Woodward DA Dobbelaere G Langsley MA Rajandream D McKeever B Shiels A Tait B Barrell N Hall, Science 2005 309 131 133 10.1126/science.1110418 15994557 (Pubitemid 40934991)
34. HaMStR: profile hidden Markov model based search for orthologs in ESTs. I Ebersberger S Strauss A von Haeseler, BMC Evol Biol 2009 9 157 10.1186/1471-2148-9-157 19586527
35. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. K Katoh K Misawa K Kuma T Miyata, Nucleic Acids Res 2002 30 3059 3066 10.1093/nar/gkf436 12136088 (Pubitemid 34851225)
36. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. J Castresana, Mol Biol Evol 2000 17 540 552 10742046 (Pubitemid 30210700)
37. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. A Stamatakis, Bioinformatics 2006 22 2688 2690 10.1093/bioinformatics/btl446 16928733 (Pubitemid 44642609)
38. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. S Whelan N Goldman, Mol Biol Evol 2001 18 691 699 11319253 (Pubitemid 32372940)
39. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. N Lartillot T Lepage S Blanquart, Bioinformatics 2009 25 2286 2288 10.1093/bioinformatics/btp368 19535536
40. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. N Lartillot H Philippe, Mol Biol Evol 2004 2 1095 1109 (Pubitemid 38658218)
41. An improved general amino-acid replacement matrix. SQ Le O Gascuel, Mol Biol Evol 2008 25 1307 1320 10.1093/molbev/msn067 18367465 (Pubitemid 351882003)
42. A genome sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation, but metabolic diversity between a gregarine and Cryptosporidium. TJ Templeton S Enomoto WJ Chen CG Huang CA Lancto MS Abrahamsen G Zhu, Mol Biol Evol 2010 27 235 248 10.1093/molbev/msp226 19778951
43. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. HA Schmidt K Strimmer M Vingron A von Haeseler, Bioinformatics 2002 18 502 504 10.1093/bioinformatics/18.3.502 11934758 (Pubitemid 34284960)
44. CONSEL: for assessing the confidence of phylogenetic tree selection. H Shimodaira M Hasegawa, Bioinformatics 2001 17 1246 1247 10.1093/bioinformatics/ 17.12.1246 11751242 (Pubitemid 33735360)
45. GeneDoc: analysis and visualization of genetic variation. KB Nicholas HBJ Nicholas DWI Deerfield, EMBnet NEWS 1997 4 14
46. WebLogo: a sequence logo generator. GE Crooks G Hon JM Chandonia SE Brenner, Genome Res 2004 14 1188 1190 10.1101/gr.849004 15173120 (Pubitemid 38811555)
47. Improved prediction of signal peptides: SignalP 3.0. JD Bendtsen H Nielsen G von Heijne S Brunak, J Mol Biol 2004 340 783 795 10.1016/j.jmb.2004. 05.028 15223320 (Pubitemid 38829638)
48. The Apicomplexan whole-genome phylogeny: an analysis of incongruence among gene trees. CH Kuo JP Wares JC Kissinger, Mol Biol Evol 2008 25 2689 2698 10.1093/molbev/msn213 18820254
49. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. G Talavera J Castresana, Syst Biol 2007 56 564 577 10.1080/10635150701472164 17654362 (Pubitemid 47171631)
50. Inferring confidence sets of possibly misspecified gene trees. K Strimmer A Rambaut, Proc Biol Sci 2002 269 137 142 10.1098/rspb.2001.1862 11798428 (Pubitemid 34107156)
51. An approximately unbiased test of phylogenetic tree selection. H Shimodaira, Syst Biol 2002 51 492 508 10.1080/10635150290069913 12079646 (Pubitemid 35180700)
52. Saturation and base composition bias explain phylogenomic conflict in Plasmodium. LM Dávalos SL Perkins, Genomics 2008 91 433 442 10.1016/j.ygeno.2008.01.006 18313259
53. Genome sequences reveal divergence times of malaria parasite lineages. JC Silva A Egan R Friedman JB Munro JM Carlton AL Hughes, Parasitology 2010 1 1 13
54. Resolving difficult phylogenetic questions: why more sequences are not enough. H Philippe H Brinkmann DV Lavrov DT Littlewood M Manuel G Wörheide D Baurain, PLoS Biol 2011 9 1000602 10.1371/journal.pbio.1000602 21423652
55. Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. AP Waters DG Higgins TF McCutchan, Proc Natl Acad Sci USA 1991 88 3140 3144 10.1073/pnas.88.8.3140 2014232 (Pubitemid 21916575)
56. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. AA Escalante FJ Ayala, Proc Natl Acad Sci USA 1995 92 5793 5797 10.1073/pnas.92.13.5793 7597031
57. Molecular phylogenetic analysis of the avian malarial parasite Plasmodium (Novyella) juxtanucleare. JC Kissinger PC Souza CO Soarest R Paul AM Wahl D Rathore TF McCutchan AU Krettli, J Parasitol 2002 88 769 773 12197128 (Pubitemid 34875703)
58. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. SL Perkins JJ Schall, J Parasitol 2002 88 972 978 12435139 (Pubitemid 35278746)
59. Evolutionary relationships between 15 Plasmodium species from new and old world primates (including humans): an 18S rDNA cladistic analysis. MC Leclerc JP Hugot P Durand F Renaud, Parasitology 2004 129 677 684 10.1017/ S0031182004006146 15648690 (Pubitemid 39657759)
60. Origins of human malaria: rare genomic changes and full mitochondrial genomes confirm the relationship of Plasmodium falciparum to other mammalian parasites but complicate the origins of Plasmodium vivax. SW Roy M Irimia, Mol Biol Evol 2008 25 1192 1198 10.1093/molbev/msn069 18359945
61. A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. ES Martinsen SL Perkins JJ Schall, Mol Phylogenet Evol 2008 47 261 273 10.1016/j.ympev.2007.11.012 18248741
62. Phylogenomics revives traditional views on deep animal relationships. H Philippe R Derelle P Lopez K Pick C Borchiellini N Boury-Esnault J Vacelet E Renard E Houliston E Quéinnec C Da Silva P Wincker H Le Guyader S Leys DJ Jackson F Schreiber D Erpenbeck B Morgenstern G Wörheide M Manuel, Curr Biol 2009 19 706 712 10.1016/j.cub.2009.02.052 19345102
63. Phylogenomics and the reconstruction of the tree of life. F Delsuc H Brinkmann H Philippe, Nat Rev Genet 2005 6 361 375 15861208 (Pubitemid 40577180)
64. Rooting phylogenetic trees with distant outgroups: a case study from the commelinoid monocots. SW Graham RG Olmstead SC Barrett, Mol Biol Evol 2002 19 1769 1781 12270903
65. The adaptation of the avian malaria parasite Plasmodium lophurae to a continuous existence in infant mice. B McGhee, J Infect Dis 1951 88 86 97 10.1093/infdis/88.1.86 14803754
66. Turning a hobby into a job: how duplicated genes find new functions. GC Conant KH Wolfe, Nat Rev Genet 2008 9 938 950 10.1038/nrg2482 19015656 (Pubitemid 352719432)
67. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. JA Boddey RL Moritz RJ Simpson AF Cowman, Traffic 2009 10 285 299 10.1111/j.1600-0854.2008.00864.x 19055692
68. Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. SH Qari YP Shi NJ Pieniazek WE Collins AA Lal, Mol Phylogenet Evol 1996 6 157 165 10.1006/mpev.1996.0068 8812316 (Pubitemid 126325593)
69. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. AA Escalante DE Freeland WE Collins AA Lal, Proc Natl Acad Sci USA 1998 95 8124 8129 10.1073/pnas.95.14.8124 9653151 (Pubitemid 28326077)
70. A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. D Rathore AM Wahl M Sullivan TF McCutchan, Mol Biochem Parasitol 2001 114 89 94 10.1016/S0166- 6851(01)00241-9 11356517 (Pubitemid 32453218)
71. SplitsTree: analyzing and visualizing evolutionary data. DH Huson, Bioinformatics 1998 14 68 73 10.1093/bioinformatics/14.1.68 9520503 (Pubitemid 28397727)