Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence

Genome Biology

Volumn 9, Issue 12, 2008, Pages

  Neafsey, Daniel E ^a   Schaffner, Stephen F ^a   Volkman, Sarah K ^b,c   Park, Daniel ^a   Montgomery, Philip ^a   Milner Jr , Danny A ^b   Lukens, Amanda ^b   Rosen, David ^b   Daniels, Rachel ^a   Houde, Nathan ^a   Cortese, Joseph F ^a   Tyndall, Erin ^a   Gates, Casey ^a   Stange Thomann, Nicole ^a   Sarr, Ousmane ^d   Ndiaye, Daouda ^d   Ndir, Omar ^d   Mboup, Soulyemane ^d   Ferreira, Marcelo U ^e   Moraes, Sandra ^e   Dash, Aditya P ^f   Chitnis, Chetan E ^g   Wiegand, Roger C ^a   Hartl, Daniel L ^h   Birren, Bruce W ^a   Lander, Eric S ^a   Sabeti, Pardis C ^a   Wirth, Dyann F ^b   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c SIMMONS COLLEGE   (United States)

^d UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f NATIONAL INSTITUTE OF MALARIA RESEARCH   (India)

^g INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^h HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC TRAIT; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HIGH THROUGHPUT SCREENING; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; POPULATION STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; ANIMAL; CLASSIFICATION; GENETIC SELECTION; GENETICS; PHYLOGENY;

PLASMODIUM FALCIPARUM;

ANIMALS; GENE FREQUENCY; GENOME-WIDE ASSOCIATION STUDY; PHYLOGENY; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION (GENETICS);

EID: 58149395271     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2008-9-12-r171     Document Type: Article

References (36)

1. Mu J Duan J Makova KD Joy DA Huynh CQ Branch OH Li WH Su XZ Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 2002, 418:323-326. 10.1038/nature00836 12124624
2. Mu J Awadalla P Duan J McGee KM Keebler J Seydel K McVean GA Su XZ Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 2007, 39:126-130. 10.1038/ng1924 17159981
3. Volkman SK Sabeti PC DeCaprio D Neafsey DE Schaffner SF Milner DA Jr Daily JP Sarr O Ndiaye D Ndir O Mboup S Duraisingh MT Lukens A Derr A Stange-Thomann N Waggoner S Onofrio R Ziaugra L Mauceli E Gnerre S Jaffe DB Zainoun J Wiegand RC Birren BW Hartl DL Galagan JE Lander ES Wirth DF A genome-wide map of diversity in Plasmodium falciparum. Nat Genet 2007, 39:113-119. 10.1038/ng1930 17159979
4. Jeffares DC Pain A Berry A Cox AV Stalker J Ingle CE Thomas A Quail MA Siebenthall K Uhlemann AC Kyes S Krishna S Newbold C Dermitzakis ET Berriman M Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet 2007, 39:120-125. 10.1038/ng1931 17159978
5. Ekland EH Fidock DA Advances in understanding the genetic basis of antimalarial drug resistance. Curr Opin Microbiol 2007, 10:363-370. 2080794 17709280 10.1016/j.mib.2007.07.007
6. Komisar JL Malaria vaccines. Front Biosci 2007 12 3928 3955 10.2741/2361 17485348
7. Howell DP Samudrala R Smith JD Disguising itself - insights into Plasmodium falciparum binding and immune evasion from the DBL crystal structure. Mol Biochem Parasitol 2006, 148, 1-9. 10.1016/ j.molbiopara.2006.03.004 16621067
8. Bisser S Ouwe-Missi-Oukem-Boyer ON Toure FS Taoufiq Z Bouteille B Buguet A Mazier D Harbouring in the brain: A focus on immune evasion mechanisms and their deleterious effects in malaria and human African trypanosomiasis. Int J Parasitol 2006, 36:529-540. 10.1016/ j.ijpara.2006.02.001 16600243
9. Ndungu FM Urban BC Marsh K Langhorne J Regulation of immune response by Plasmodium-infected red blood cells. Parasite Immunol 2005, 27:373-384. 10.1111/j.1365-3024.2005.00771.x 16179031
10. Anderson TJ Haubold B Williams JT Estrada-Franco JG Richardson L Mollinedo R Bockarie M Mokili J Mharakurwa S French N Whitworth J Velez ID Brockman AH Nosten F Ferreira MU Day KP Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 2000, 17:1467-1482. 11018154
11. Wootton JC Feng X Ferdig MT Cooper RA Mu J Baruch DI Magill AJ Su XZ Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 2002, 418:320-323. 10.1038/nature00813 12124623
12. Mu J Awadalla P Duan J McGee KM Joy DA McVean GA Su XZ Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol 2005, 3:e335. 1201364 16144426 10.1371/journal.pbio.0030335
13. Kidgell C Volkman SK Daily J Borevitz JO Plouffe D Zhou Y Johnson JR Le Roch K Sarr O Ndir O Mboup S Batalov S Wirth DF Winzeler EA A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog 2006, 2:e57. 1480597 16789840 10.1371/journal.ppat.0020057
14. Huentelman MJ Craig DW Shieh AD Corneveaux JJ Hu-Lince D Pearson JV Stephan DA SNiPer: Improved SNP genotype calling for Affymetrix 10 K GeneChip microarray data. BMC Genomics 2005, 6:149. 1280925 16262895 10.1186/1471-2164-6-149
15. PlasmoDB: The Plasmodium Genome Resource http://www.plasmodb.org
16. Ben-Ari G Zenvirth D Sherman A Simchen G Lavi U Hillel J Application of SNPs for assessing biodiversity and phylogeny among yeast strains. Heredity 2005, 95:493-501. 10.1038/sj.hdy.6800759 16175193
17. Gardner MJ Hall N Fung E White O Berriman M Hyman RW Carlton JM Pain A Nelson KE Bowman S Paulsen IT James K Eisen JA Rutherford K Salzberg SL Craig A Kyes S Chan MS Nene V Shallom SJ Suh B Peterson J Angiuoli S Pertea M Allen J Selengut J Haft D Mather MW Vaidya AB Martin DM et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511. 10.1038/nature01097 12368864
18. Pritchard JK Stephens M Donnelly P Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959. 1461096 10835412
19. Patterson N Price AL Reich D Population structure and eigenanalysis. PLoS Genet 2006, 2:e190. 1713260 17194218 10.1371/journal.pgen.0020190
20. Machado RL Povoa MM Calvosa VS Ferreira MU Rossit AR dos Santos EJ Conway DJ Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis 2004. 190:1547-1555. 10.1086/ 424601 15478058
21. Maynard Smith J Haigh J The hitch-hiking effect of a favourable gene. Genet Res 1974, 23:23-35. 4407212
22. Fay JC Wu CI Hitchhiking under positive Darwinian selection. Genetics 2000, 155:1405-1413. 1461156 10880498
23. Anderson TJ Nair S Sudimack D Williams JT Mayxay M Newton PN Guthmann JP Smithuis FM Tran TH Broek van den IV White NJ Nosten F Geographical distribution of selected and putatively neutral SNPs in Southeast Asian malaria parasites. Mol Biol Evol 2005, 22:2362-2374. 10.1093/molbev/ msi235 16093566
24. Frazer KA Ballinger DG Cox DR Hinds DA Stuve LL Gibbs RA Belmont JW Boudreau A Hardenbol P Leal SM Pasternak S Wheeler DA Willis TD Yu F Yang H Zeng C Gao Y Hu H Hu W Li C Lin W Liu S Pan H Tang X Wang J Wang W Yu J Zhang B Zhang Q Zhao H et al. A second generation human haplotype map of over 3.1 million SNPs. Nature 2007, 449:851-861. 10.1038/ nature06258 17943122
25. Barreiro LB Laval G Quach H Patin E Quintana-Murci L Natural selection has driven population differentiation in modern humans. Nat Genet 2008, 40:340-345. 10.1038/ng.78 18246066
26. Polley SD Conway DJ Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 2001, 158:1505-1512. 1461755 11514442
27. Verra F Hughes AL Natural selection on apical membrane antigen-1 of Plasmodium falciparum. Parassitologia 1999, 41:93-95. 10697839
28. Ferreira MU Ribeiro WL Tonon AP Kawamoto F Rich SM Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene 2003, 304:65-75. 10.1016/S0378-1119(02)01180-0 12568716
29. Sabeti PC Reich DE Higgins JM Levine HZ Richter DJ Schaffner SF Gabriel SB Platko JV Patterson NJ McDonald GJ Ackerman HC Campbell SJ Altshuler D Cooper R Kwiatkowski D Ward R Lander ES Detecting recent positive selection in the human genome from haplotype structure. Nature 2002, 419:832-837. 10.1038/nature01140 12397357
30. Nair S Nash D Sudimack D Jaidee A Barends M Uhlemann AC Krishna S Nosten F Anderson TJ Recurrent gene amplification and soft selective sweeps during evolution of multidrug resistance in malaria parasites. Mol Biol Evol 2007, 24:562-573. 10.1093/molbev/msl185 17124182
31. Nair S Williams JT Brockman A Paiphun L Mayxay M Newton PN Guthmann JP Smithuis FM Hien TT White NJ Nosten F Anderson TJ A selective sweep driven by pyrimethamine treatment in southeast asian malaria parasites. Mol Biol Evol 2003, 20:1526-1536. 10.1093/molbev/msg162 12832643
32. Nash D Nair S Mayxay M Newton PN Guthmann JP Nosten F Anderson TJ Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci 2005, 272:1153-1161. 1559806 16024377 10.1098/ rspb.2004.3026
33. Hudson RR Slatkin M Maddison WP Estimation of levels of gene flow from DNA sequence data. Genetics 1992, 132:583-589. 1205159 1427045
34. Guindon S Gascuel O A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 10.1080/10635150390235520 14530136
35. Gascuel O BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 1997, 14:685-695. 9254330
36. Baniecki ML Wirth DF Clardy J High-throughput Plasmodium falciparum growth assay for malaria drug discovery. Antimicrob Agents Chemother 2007, 51:716-723. 1797774 17116676 10.1128/AAC.01144-06