Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum

Molecular Biology and Evolution

Volumn 27, Issue 10, 2010, Pages 2344-2351

  Ochola, Lynette Isabella ^a   Tetteh, Kevin K A ^b   Stewart, Lindsay B ^b   Riitho, Victor ^a   Marsh, Kevin ^a   Conway, David J ^b  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

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

Author keywords

allele frequency; antigens; immunity; polymorphism and divergence; tests of neutrality

Indexed keywords

ARTICLE; GENE FREQUENCY; GENE LOCUS; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; IMMUNITY; KENYA; NONHUMAN; PLASMODIUM; PLASMODIUM FALCIPARUM; PLASMODIUM REICHENOWI; POPULATION GENETICS; SAMPLE SIZE; SINGLE NUCLEOTIDE POLYMORPHISM;

COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENES, PROTOZOAN; GENETIC VARIATION; GENETICS, POPULATION; GENOMICS; HUMANS; KENYA; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SPECIES SPECIFICITY;

PAN; PLASMODIUM FALCIPARUM; PLASMODIUM REICHENOWI;

EID: 77957242593     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq119     Document Type: Article

References (48)

1. Andres AM, Hubisz MJ, Indap A, et al. (12 co-authors). 2009. Targets of balancing selection in the human genome. Mol Biol Evol. 26:2755-2764.
2. Aurrecoechea C, Brestelli J, Brunk BP, et al. (25 co-authors). 2009. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37:D539-D543.
3. Baum J, Thomas AW, Conway DJ. 2003. Evidence for diversifying selection on erythrocyte-binding antigens of Plasmodium falciparum and P. vivax. Genetics 163:1327-1336.
4. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:85-100.
5. Bubb KL, Bovee D, Buckley D, et al. (12 co-authors). 2006. Scan of human genome reveals no new loci under ancient balancing selection. Genetics 173:2165-2177.
6. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:e64.
7. Cheeseman IH, Gomez-Escobar N, Carret CK, Ivens A, Stewart LB, Tetteh KK, Conway DJ. 2009. Gene copy number variation throughout the Plasmodium falciparum genome. BMC Genomics. 10:353.
8. Cheesman S, Tanabe K, Sawai H, O'Mahony E, Carter R. 2009. Strain-specific immunity may drive adaptive polymorphism in the merozoite surface protein 1 of the rodent malaria parasite Plasmodium chabaudi. Infect Genet Evol. 9:248-255.
9. Conway DJ. 1997. Natural selection on polymorphic malaria antigens and the search for a vaccine. Parasitol Today. 13:26-29.
10. Conway DJ, Cavanagh DR, Tanabe K, et al. (12 co-authors). 2000. A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses. Nat Med. 6:689-692.
11. Conway DJ, Polley SD. 2002. Measuring immune selection. Parasitology 125:S3-S16.
12. Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF. 2003. Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plas-modium falciparum vaccine candidate AMA1. Infect Immun. 71:1416-1426.
13. Ferreira MU, Hartl DL. 2007. Plasmodium falciparum: worldwide sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-2 (MSP-2). Exp Parasitol. 115:32-40.
14. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
15. Hayton K, Gaur D, Liu A, et al. (15 co-authors). 2008. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe. 4:40-51.
16. Hill WG, Robertson A. 1968. Linkage disequilibrium in finite populations. Theor Appl Genet. 38:226-231.
17. Hudson RR, Kreitman R, Aguade M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
18. Innan H. 2006. Modified Hudson-Kreitman-Aguade test and two-dimensional evaluation of neutrality tests. Genetics. 173:1725-1733.
19. Jeffares DC, Pain A, Berry A, et al. (15 co-authors). 2007. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet. 39:120-125.
20. Joy DA, Feng X, Mu J, et al. (12 co-authors). 2003. Early origin and recent expansion of Plasmodium falciparum. Science 300:318-321.
21. Kidgell C, Volkman SK, Daily J, et al. (14 co-authors). 2006. A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog. 2:e57.
22. Krief S, Escalante AA, Pacheco MA, et al. (18 co-authors). 2010. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 6:e1000765.
23. Llinas M, Bozdech Z, Wong ED, Adai AT, DeRisi JL. 2006. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 34:1166-1173.
24. Mackinnon MJ, Li J, Mok S, Kortok MM, Marsh K, Preiser PR, Bozdech Z. 2009. Comparative transcriptional and genomic analysis of Plasmodium falciparum field isolates. PLoS Pathog. 5:e1000644.
25. Martinelli A, Cheesman S, Hunt P, Culleton R, Raza A, Mackinnon M, Carter R. 2005. A genetic approach to the de novo identification of targets of strain-specific immunity in malaria parasites. Proc Natl Acad Sci\USA. 102:814-819.
26. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
27. Mphande FA, Ribacke U, Kaneko O, Kironde F, Winter G, Wahlgren M. 2008. SURFIN4.1, a schizont-merozoite associated protein in the SURFIN family of Plasmodium falciparum. Malar J. 7:116.
28. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, Seydel K, McVean GA, Su XZ. 2007. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet. 39:126-130.
29. Mwangi TW, Fegan G, Williams TN, Kinyanjui SM, Snow RW, Marsh K. 2008. Evidence for over-dispersion in the distribution of clinical malaria episodes in children. PLoS One. 3:e2196.
30. Nielsen R. 2001. Statistical tests of selective neutrality in the age of genomics. Heredity 86:641-647.
31. Pattaradilokrat S, Cheesman SJ, Carter R. 2007. Linkage group selection: towards identifying genes controlling strain specific protective immunity in malaria. PLoS One. 2:e857.
32. Polley SD, Chokejindachai W, Conway DJ. 2003. Allele frequency based analyses robustly identify sites under balancing selection in a malaria vaccine candidate antigen. Genetics. 165:555-561.
33. Polley SD, Conway DJ. 2001. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158:1505-1512.
34. Polley SD, Tetteh KK, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, Conway DJ. 2007. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis. 195:279-287.
35. Prugnolle F, Durand P, Neel C, et al. (13 co-authors). 2010. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci\USA. 107:1458-1463.
36. Ribacke U, Mok BW, Wirta V, Normark J, Lundeberg J, Kironde F, Egwang TG, Nilsson P, Wahlgren M. 2007. Genome wide gene amplifications and deletions in Plasmodium falciparum. Mol Biochem Parasitol. 155:33-44.
37. Rozas J. 2009. DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol. 537:337-350.
38. Singh S, Soe S, Weisman S, Barnwell JW, Perignon JL, Druilhe P. 2009. A conserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum. PLoS One. 4:e5410.
39. Tajima F. 1989a. DNA polymorphism in a subdivided population: the expected number of segregating sites in the two-subpopulation model. Genetics 123:229-240.
40. Tajima F. 1989b. The effect of change in population size on DNA polymorphism. Genetics 123:597-601.
41. Tajima F. 1989c. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
42. Tetteh KK, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, Marsh K, Weedall GD, Conway DJ. 2009. Prospective identification of malaria parasite genes under balancing selection. PLoS One. 4:e5568.
43. Verra F, Chokejindachai W, Weedall GD, Polley SD, Mwangi TW, Marsh K, Conway DJ. 2006. Contrasting signatures of selection on the Plasmodium falciparum erythrocyte binding antigen gene family. Mol Biochem Parasitol. 149:182-190.
44. Volkman SK, Sabeti PC, DeCaprio D, et al. (28 co-authors). 2007. A genome-wide map of diversity in Plasmodium falciparum. Nat Genet. 39:113-119.
45. Weedall GD, Preston BM, Thomas AW, Sutherland CJ, Conway DJ. 2007. Differential evidence of natural selection on two leading sporozoite stage malaria vaccine candidate antigens. Int J Parasitol. 37:77-85.
46. Wickramarachchi T, Cabrera AL, Sinha D, et al. (11 co-authors). 2009. A novel Plasmodium falciparum erythrocyte binding protein associated with the merozoite surface, PfDBLMSP. Int J Parasitol. 39:763-773.
47. Winter G, Kawai S, Haeggstrom M, Kaneko O, von Euler A, Kawazu S, Palm D, Fernandez V, Wahlgren M. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med. 201: 1853-1863.
48. Zhai W, Nielsen R, Slatkin M. 2009. An investigation of the statistical power of neutrality tests based on comparative and population genetic data. Mol Biol Evol. 26:273-283.