Gene-specific signatures of elevated non-synonymous substitution rates correlate poorly across the Plasmodium genus

PLoS ONE

Volumn 3, Issue 5, 2008, Pages

  Weedall, Gareth D ^a   Polley, Spencer D ^a   Conway, David J ^a,b  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND;

ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE MUTATION; GENE SEQUENCE; GENETIC REGULATION; GENOME; GENUS; NONHUMAN; ORTHOLOGY; PHYLOGENY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM REICHENOWI; PLASMODIUM VIVAX; PLASMODIUM YOELII; PREDICTION; PROTOZOAL GENETICS; PROTOZOON; SPECIES DIFFERENCE; ANIMAL; CLASSIFICATION; GENE; GENETICS;

PAN; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM REICHENOWI; PLASMODIUM VIVAX; PLASMODIUM YOELII;

ANIMALS; GENES, PROTOZOAN; PHYLOGENY; PLASMODIUM; SPECIES SPECIFICITY;

EID: 48449087547     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002281     Document Type: Article

References (78)

1. Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity 86: 641-647.
2. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
3. Jeffares DC, Pain A, Berry A, Cox AV, Stalker J, et al. (2007) Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet 39: 120-125.
4. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, et al. (2007) Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 39: 126-130.
5. Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, et al. (2007) A genome-wide map of diversity in Plasmodium falciparum. Nat Genet 39: 113-119.
6. Hughes AL, Friedman R (2005) Amino acid sequence constraint and gene expression pattern across the life history in the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 142: 170-176.
7. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, et al. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82-86.
8. Mu J, Duan J, Makova KD, Joy DA, Huynh CQ, et al. (2002) Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418: 323-326.
9. Stoeckert CJ Jr, Fischer S, Kissinger JC, Heiges M, Aurrecoechea C, et al. (2006) PlasmoDB v5: new looks, new genomes. Trends Parasitol 22: 543-546.
10. Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88: 972-978.
11. Arisue N, Hirai M, Arai M, Matsuoka H, Horii T (2007) Phylogeny and evolution of the SERA multigene family in the genus Plasmodium. J Mol Evol 65: 82-91.
12. Rich SM, Ayala FJ (2003) Progress in malaria research: the case for phylogenetics. Adv Parasitol 54: 255-280.
13. Escalante AA, Ayala FJ (1994) Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci USA 91: 11373-11377.
14. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
15. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, et al. (2002) Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419: 512-519.
16. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
17. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34: W609-612.
18. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
19. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17: 32-43.
20. Marshall VM, Silva A, Foley M, Cranmer S, Wang L, et al. (1997) A second merozoite surface protein (MSP-4) of Plasmodium falciparum that contains an epidermal growth factor-like domain. Infect Immun 65: 4460-4467.
21. Sanders PR, Kats LM, Drew DR, O'Donnell RA, O'Neill M, et al. (2006) A set of glycosylphosphatidyl inositol-anchored membrane proteins of Plasmodium falciparum is refractory to genetic deletion. Infect Immun 74: 4330-4338.
22. Marshall VM, Tieqiao W, Coppel RL (1998) Close linkage of three merozoite surface protein genes on chromosome 2 of Plasmodium falciparum. Mol Biochem Parasitol 94: 13-25.
23. Muller HM, Reckmann I, Hollingdale MR, Bujard H, Robson KJ, et al. (1993) Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. Embo J 12: 2881-2889.
24. Sultan AA, Thathy V, Frevert U, Robson KJ, Crisanti A, et al. (1997) TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90: 511-522.
25. McCormick CJ, Tuckwell DS, Crisanti A, Humphries MJ, Hollingdale MR (1999) Identification of heparin as a ligand for the A-domain of Plasmodium falciparum thrombospondin-related adhesion protein. Mol Biochem Parasitol 100: 111-124.
26. Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, et al. (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9: 87-92.
27. Narum DL, Fuhrmann SR, Luu T, Sim BK (2002) A novel Plasmodium falciparum erythrocyte binding protein-2 (EBP2/BAEBL) involved in erythrocyte receptor binding. Mol Biochem Parasitol 119: 159-168.
28. Thompson JK, Triglia T, Reed MB, Cowman AF (2001) A novel ligand from Plasmodium falciparum that binds to a sialic acid-containing receptor on the surface of human erythrocytes. Mol Microbiol 41: 47-58.
29. Pearce JA, Mills K, Triglia T, Cowman AF, Anders RF (2005) Characterisation of two novel proteins from the asexual stage of Plasmodium falciparum, H101 and H103. Mol Biochem Parasitol 139: 141-151.
30. Ghai M, Dutta S, Hall T, Freilich D, Ockenhouse CF (2002) Identification, expression, and functional characterization of MAEBL, a sporozoite and asexual blood stage chimeric erythrocyte-binding protein of Plasmodium falciparum. Mol Biochem Parasitol 123: 35-45.
31. Kariu T, Yuda M, Yano K, Chinzei Y (2002) MAEBL is essential for malarial sporozoite infection of the mosquito salivary gland. J Exp Med 195: 1317-1323.
32. Preiser P, Renia L, Singh N, Balu B, Jarra W, et al. (2004) Antibodies against MAEBL ligand domains M1 and M2 inhibit sporozoite development in vitro. Infect Immun 72: 3604-3608.
33. Gilberger T-M, Thompson JK, Triglia T, Good RT, Duraisingh MT, et al. (2003) A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem 278: 14480-14486.
34. Howard RF, Reese RT (1990) Plasmodium falciparum: hetero-oligomeric complexes of rhoptry polypeptides. Exp Parasitol 71: 330-342.
35. Ridley RG, Lahm H-W, Takacs B, Scaife JG (1991) Genetic and structural relationships between components of a protective rhoptry antigen complex from Plasmodium falciparum. Mol Biochem Parasitol 47: 245-247.
36. Hisaeda H, Stowers AW, Tsuboi T, Collins WE, Sattabongkot JS, et al. (2000) Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 68: 6618-6623.
37. Tomas AM, Margos G, Dimopoulos G, van Lin LH, de Koning-Ward TF, et al. (2001) P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. Embo J 20: 3975-3983.
38. van Schaijk BC, van Dijk MR, van de Vegte-Bolmer M, van Gemert GJ, van Dooren MW, et al. (2006) Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol Biochem Parasitol 149: 216-222.
39. Gaur D, Singh S, Jiang L, Diouf A, Miller LH (2007) Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc Natl Acad Sci U S A 104: 17789-17794.
40. Kaneko O, Mu J, Tsuboi T, Su X, Torii M (2002) Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins. Mol Biochem Parasitol 121: 275-278.
41. Stubbs J, Simpson KM, Triglia T, Plouffe D, Tonkin CJ, et al. (2005) Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309: 1384-1387.
42. Ishino T, Chinzei Y, Yuda M (2005) Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 58: 1264-1275.
43. Sterkers Y, Scheidig C, da Rocha M, Lepolard C, Gysin J, et al. (2007) Members of the low-molecular-mass rhoptry protein complex of Plasmodium falciparum bind to the surface of normal erythrocytes. J Infect Dis 196: 617-621.
44. Sanders PR, Gilson PR, Cantin GT, Greenbaum DC, Nebl T, et al. (2005) Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J Biol Chem 280: 40169-40176.
45. Black CG, Wang L, Wu T, Coppel RL (2003) Apical location of a novel EGF-like domain-containing protein of Plasmodium falciparum. Mol Biochem Parasitol 127: 59-68.
46. Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A, et al. (2004) A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 279: 9490-9496.
47. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, et al. (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38: 706-718.
48. Kato K, Mayer DC, Singh S, Reid M, Miller LH (2005) Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx. Proc Natl Acad Sci U S A 102: 5552-5557.
49. Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M (2006) CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol 59: 1369-1379.
50. Borre MB, Dziegiel M, Hogh B, Petersen E, Rieneck K, et al. (1991) Primary structure and localization of a conserved immunogenic Plasmodium falciparum glutamate rich protein (GLURP) expressed in both the preerythrocytic and erythrocytic stages of the vertebrate life cycle. Mol Biochem Parasitol 49: 119-131.
51. Trenholme KR, Gardiner DL, Holt DC, Thomas EA, Cowman AF, et al. (2000) clag9: A cytoadherence gene in Plasmodium falciparum essential for binding of parasitized erythrocytes to CD36. Proc Natl Acad Sci U S A 97: 4029-4033.
52. Ling IT, Florens L, Dluzewski AR, Kaneko O, Grainger M, et al. (2004) The Plasmodium falciparum clag9 gene encodes a rhoptry protein that is transferred to the host erythrocyte upon invasion. Mol Microbiol 52: 107-118.
53. Yuda M, Sakaida H, Chinzei Y (1999) Targeted disruption of the Plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J Exp Med 190: 1711-1716.
54. Dessens JT, Beetsma AL, Dimopoulos G, Wengelnik K, Crisanti A, et al. (1999) CTRP is essential for mosquito infection by malaria ookinetes. Embo J 18: 6221-6227.
55. Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, et al. (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177: 1287-1298.
56. Cerami C, Frevert U, Sinnis P, Takacs B, Clavijo P, et al. (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70: 1021-1033.
57. Sidjanski SP, Vanderberg JP, Sinnis P (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 90: 33-41.
58. Ling IT, Kaneko O, Narum DL, Tsuboi T, Howell S, et al. (2003) Characterisation of the rhoph2 gene of Plasmodium falciparum and Plasmodium yoelii. Mol Biochem Parasitol 127: 47-57.
59. van Dijk MR, Janse CJ, Thompson J, Waters AP, Braks JA, et al. (2001) A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153-164.
60. Cowman AF, Baldi DL, Healer J, Mills KE, O'Donnell RA, et al. (2000) Functional analysis of proteins involved in Plasmodium falciparum merozoite invasion of red blood cells. FEBS Lett 476: 84-88.
61. Lustigman S, Anders RF, Brown GV, Coppel RL (1988) A component of an antigenic rhoptry complex of Plasmodium falciparum is modified after merozoite invasion. Mol Biochem Parasitol 30: 217-224.
62. Dessens JT, Mendoza J, Claudianos C, Vinetz JM, Khater E, et al. (2001) Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect Immun 69: 4041-4047.
63. Tsai YL, Hayward RE, Langer RC, Fidock DA, Vinetz JM (2001) Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun 69: 4048-4054.
64. Thompson J, Cooke RE, Moore S, Anderson LF, Janse CJ, et al. (2004) PTRAMP; a conserved Plasmodium thrombospondin-related apical merozoite protein. Mol Biochem Parasitol 134: 225-232.
65. Topolska AE, Lidgett A, Truman D, Fujioka H, Coppel RL (2004) Characterization of a membrane-associated rhoptry protein of Plasmodium falciparum. J Biol Chem 279: 4648-4656.
66. Eksi S, Czesny B, van Gemert GJ, Sauerwein RW, Eling W, et al. (2006) Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol Microbiol 61: 991-998.
67. Quakyi IA, Carter R, Rener J, Kumar N, Good MF, et al. (1987) The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. J Immunol 139: 4213-4217.
68. Kaneko O, Yim Lim BY, Iriko H, Ling IT, Otsuki H, et al. (2005) Apical expression of three RhopH1/Clag proteins as components of the Plasmodium falciparum RhopH complex. Mol Biochem Parasitol 143: 20-28.
69. Chattopadhyay R, Rathore D, Fujioka H, Kumar S, de la Vega P, et al. (2003) PfSPATR, a Plasmodium falciparum protein containing an altered thrombospondin type I repeat domain is expressed at several stages of the parasite life cycle and is the target of inhibitory antibodies. J Biol Chem 278: 25977-25981.
70. Burns JM Jr, Adeeku EK, Dunn PD (1999) Protective immunization with a novel membrane protein of Plasmodium yoelii-infected erythrocytes. Infect Immun 67: 675-680.
71. Dessens JT, Siden-Kiamos I, Mendoza J, Mahairaki V, Khater E, et al. (2003) SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49: 319-329.
72. Yuda M, Yano K, Tsuboi T, Torii M, Chinzei Y (2001) von Willebrand Factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout Plasmodium parasites. Mol Biochem Parasitol 116: 65-72.
73. Shi Q, Cernetich-Ott A, Lynch MM, Burns JM Jr (2006) Expression, localization, and erythrocyte binding activity of Plasmodium yoelii merozoite surface protein-8. Mol Biochem Parasitol 149: 231-241.
74. Kadota K, Ishino T, Matsuyama T, Chinzei Y, Yuda M (2004) Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci U S A 101: 16310-16315.
75. Kushwaha A, Perween A, Mukund S, Majumdar S, Bhardwaj D, et al. (2002) Amino terminus of Plasmodium falciparum acidic basic repeat antigen interacts with the erythrocyte membrane through band 3 protein. Mol Biochem Parasitol 122: 45-54.
76. Li X, Chen H, Oo TH, Daly TM, Bergman LW, et al. (2004) A co-ligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3. J Biol Chem 279: 5765-5771.
77. Ishino T, Orito Y, Chinzei Y, Yuda M (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59: 1175-1184.
78. Siden-Kiamos I, Ecker A, Nyback S, Louis C, Sinden RE, et al. (2006) Plasmodium berghei calcium-dependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol Microbiol 60: 1355-1363.