Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Large-scale Genotyping and Genetic Mapping in Plasmodium Parasites

  • Su, Xin-Zhuan (Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institute of Health) ;
  • Jiang, Hongying (Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institute of Health) ;
  • Yi, Ming (Advanced Technology Program, SAIC-Frederick, Inc., NCI-Frederick) ;
  • Mu, Jianbing (Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institute of Health) ;
  • Stephens, Robert M. (Advanced Technology Program, SAIC-Frederick, Inc., NCI-Frederick)
  • Published : 2009.06.30
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Abstract

The completion of many malaria parasite genomes provides great opportunities for genomewide characterization of gene expression and high-throughput genotyping. Substantial progress in malaria genomics and genotyping has been made recently, particularly the development of various microarray platforms for large-scale characterization of the Plasmodium falciparum genome. Microarray has been used for gene expression analysis, detection of single nucleotide polymorphism (SNP) and copy number variation (CNV), characterization of chromatin modifications, and other applications. Here we discuss some recent advances in genetic mapping and genomic studies of malaria parasites, focusing on the use of high-throughput arrays for the detection of SNP and CNV in the P. falciparum genome. Strategies for genetic mapping of malaria traits are also discussed.

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References

  1. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 2005; 434: 214-217 https://doi.org/10.1038/nature03342
  2. Cox J, Hay SI, Abeku TA, Checchi F, Snow RW. The uncertain burden of Plasmodium falciparum epidemics in Africa. Trends Parasitol 2007; 23: 142-148 https://doi.org/10.1016/j.pt.2007.02.002
  3. Mendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 2001; 64 (1-2 Suppl): 97-106 https://doi.org/10.4269/ajtmh.2001.64.97
  4. Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 2008; 5: e127 https://doi.org/10.1371/journal.pmed.0050127
  5. Perkins SL, Schall JJ. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 2002; 88: 972-978 https://doi.org/10.1645/0022-3395(2002)088[0972:AMPOMP]2.0.CO;2
  6. Carlton J, Silva J, Hall N. The genome of model malaria parasites, and comparative genomics. Curr Issues Mol Biol 2005; 7: 23-37
  7. 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, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002; 419: 498-511 https://doi.org/10.1038/nature01097
  8. Hall N, Carlton J. Comparative genomics of malaria parasites. Curr Opin Genet Dev 2005; 15: 609-613 https://doi.org/10.1016/j.gde.2005.09.001
  9. Pollack Y, Katzen AL, Spira DT, Golenser J. The genome of Plasmodium falciparum. I. DNA base composition. Nucleic Acids Res 1982; 10: 539-546 https://doi.org/10.1093/nar/10.2.539
  10. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RM, Crabb BS, Del Portillo HA, Essien K, Feldblyum TV, Fernandez-Becerra C, Gilson PR, Gueye AH, Guo X, Kang'a S, Kooij TW, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, Salzberg SL, Stoeckert CJ, Sullivan SA, Yamamoto MM, Hoffman SL, Wortman JR, Gardner MJ, Galinski MR, Barnwell JW, Fraser-Liggett CM. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008; 455: 757-763 https://doi.org/10.1038/nature07327
  11. Carter R, Voller A. Enzyme variants in primate malaria parasites. Trans R Soc Trop Med Hyg 1973; 67: 14-15 https://doi.org/10.1016/0035-9203(73)90274-5
  12. Walliker D, Sanderson A, Yoeli M, Hargreaves BJ. A genetic investigation of virulence in a rodent malaria parasite. Parasitology 1976; 72: 183-194 https://doi.org/10.1017/S0031182000048484
  13. Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 1987; 236: 1661-1666 https://doi.org/10.1126/science.3299700
  14. Wellems TE, Panton LJ, Gluzman IY, do Rosario VE, Gwadz RW, Walker-Jonah A, Krogstad DJ. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature 1990; 345: 253-255 https://doi.org/10.1038/345253a0
  15. Su XZ, Wellems TE. Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics 1996; 33: 430-444 https://doi.org/10.1006/geno.1996.0218
  16. Su XZ, Kirkman LA, Fujioka H, Wellems TE. Complex polymorphisms in an approximately 330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. Cell 1997; 91: 593-603 https://doi.org/10.1016/S0092-8674(00)80447-X
  17. Maresso K, Broeckel U. Genotyping platforms for mass-throughput genotyping with SNPs, including human genome-wide scans. Adv Genet 2008; 60: 107-139 https://doi.org/10.1016/S0065-2660(07)00405-1
  18. Su XZ, Hayton K, Wellems TE. Genetic linkage and association analyses for trait mapping in Plasmodium falciparum. Nat Rev Genet 2007; 8: 497-506 https://doi.org/10.1038/nrg2126
  19. Su XZ, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, Wootton JC, Wellems TE. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science 1999; 286: 1351-1353 https://doi.org/10.1126/science.286.5443.1351
  20. 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 https://doi.org/10.1038/ng1931
  21. 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 https://doi.org/10.1038/ng1924
  22. 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 https://doi.org/10.1038/ng1930
  23. Grech K, Martinelli A, Pathirana S, Walliker D, Hunt P, Carter R. Numerous, robust genetic markers for Plasmodium chabaudi by the method of amplified fragment length polymorphism. Mol Biochem Parasitol 2002; 123: 95-104 https://doi.org/10.1016/S0166-6851(02)00142-1
  24. Feng X, Carlton JM, Joy DA, Mu J, Furuya T, Suh BB, Wang Y, Barnwell JW, Su XZ. Single-nucleotide polymorphisms and genome diversity in Plasmodium vivax. Proc Natl Acad Sci USA 2003; 100: 8502-8507 https://doi.org/10.1073/pnas.1232502100
  25. Martinelli A, Hunt P, Cheesman SJ, Carter R. Amplified fragment length polymorphism measures proportions of malaria parasites carrying specific alleles in complex genetic mixtures. Mol Biochem Parasitol 2004; 136: 117-122 https://doi.org/10.1016/j.molbiopara.2004.02.011
  26. Li J, Zhang Y, Sullivan M, Hong L, Huang L, Lu F, McCutchan TF, Su XZ. Typing Plasmodium yoelii microsatellites using a simple and affordable fluorescent labeling method. Mol Biochem Parasitol 2007; 155: 94-102 https://doi.org/10.1016/j.molbiopara.2007.06.003
  27. Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 2008; 410: 105-112 https://doi.org/10.1016/j.gene.2007.11.022
  28. Anderson TJ, Su XZ, Roddam A, Day KP. Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol Ecol 2000; 9: 1599-1608 https://doi.org/10.1046/j.1365-294x.2000.01057.x
  29. 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 https://doi.org/10.1038/nature00813
  30. Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. Intercontinental spread of pyrimethamine-resistant malaria. Science 2004; 305: 1124 https://doi.org/10.1126/science.1098876
  31. Anderson TJ. Mapping drug resistance genes in Plasmodium falciparum by genome-wide association. Curr Drug Targets Infect Disord 2004; 4: 65-78 https://doi.org/10.2174/1568005043480943
  32. Mu J, Duan J, Makova K, 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 https://doi.org/10.1038/nature00836
  33. Volkman SK, Hartl DL, Wirth DF, Nielsen KM, Choi M, Batalov S, Zhou Y, Plouffe D, Le Roch KG, Abagyan R, Winzeler EA. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 2002; 298: 216-218 https://doi.org/10.1126/science.1075642
  34. Mu J, Ferdig MT, Feng X, Joy DA, Duan J, Furuya T, Subramanian G, Aravind L, Cooper RA, Wootton JC, Xiong M, Su XZ. Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol Microbiol 2003; 49: 977-989 https://doi.org/10.1046/j.1365-2958.2003.03627.x
  35. Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF, Hartl DL. Recent origin of Plasmodium falciparum from a single progenitor. Science 2001; 293: 482-484 https://doi.org/10.1126/science.1059878
  36. 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 https://doi.org/10.1371/journal.ppat.0020057
  37. Rich SM, Licht MC, Hudson RR, Ayala FJ. Malaria's Eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci USA 1998; 95: 4425-4430 https://doi.org/10.1073/pnas.95.8.4425
  38. Hughes AL, Verra F. Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc R Soc Lond B Biol Sci 2001; 268: 1855-1860 https://doi.org/10.1098/rspb.2001.1759
  39. 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 https://doi.org/10.1093/oxfordjournals.molbev.a026247
  40. Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, Dorsey G. Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. Am J Trop Med Hyg 2006; 75: 836-842
  41. Dolan SA, Herrfeldt JA, Wellems TE. Restriction polymorphisms and fingerprint patterns from an interspersed repetitive element of Plasmodium falciparum DNA. Mol Biochem Parasitol 1993; 61: 137-142 https://doi.org/10.1016/0166-6851(93)90166-U
  42. Su XZ, Wellems TE. Plasmodium falciparum: a rapid DNA fingerprinting method using microsatellite sequences within var clusters. Exp Parasitol 1997; 86: 235-236 https://doi.org/10.1006/expr.1997.4174
  43. Su XZ, Carucci DJ, Wellems TE. Plasmodium falciparum: parasite typing by using a multicopy microsatellite marker, PfRRM. Exp Parasitol 1998; 89: 262-265 https://doi.org/10.1006/expr.1998.4299
  44. Ferdig MT, Su XZ. Microsatellite markers and genetic mapping in Plasmodium falciparum. Parasitol Today 2000; 16: 307-312 https://doi.org/10.1016/S0169-4758(00)01676-8
  45. Crameri A, Marfurt J, Mugittu K, Maire N, Rego_s A, Coppee JY, Sismeiro O, Burki R, Huber E, Laubscher D, Puijalon O, Genton B, Felger I, Beck HP. Rapid microarray-based method for monitoring of all currently known single-nucleotide polymorphisms associated with parasite resistance to antimalaria drugs. J Clin Microbiol 2007; 45: 3685-3691 https://doi.org/10.1128/JCM.01178-07
  46. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 2008; 7: 223 https://doi.org/10.1186/1475-2875-7-223
  47. Lindblad-Toh K, Winchester E, Daly MJ, Wang DG, Hirschhorn JN, Laviolette JP, Ardlie K, Reich DE, Robinson E, Sklar P, Shah N, Thomas D, Fan JB, Gingeras T, Warrington J, Patil N, Hudson TJ, Lander ES. Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse. Nat Genet 2000; 24: 381-386 https://doi.org/10.1038/74215
  48. Kennedy GC, Matsuzaki H, Dong S, Liu WM, Huang J, Liu G, Su X, Cao M, Chen W, Zhang J, Liu W, Yang G, Di X, Ryder T, He Z, Surti U, Phillips MS, Boyce-Jacino MT, Fodor SP, Jones KW. Largescale genotyping of complex DNA. Nat Biotechnol 2003; 21: 1233-1237 https://doi.org/10.1038/nbt869
  49. Gunderson KL, Steemers FJ, Lee G, Mendoza LG, Chee MS. A genome-wide scalable SNP genotyping assay using microarray technology. Nat Genet 2005; 37: 549-554 https://doi.org/10.1038/ng1547
  50. Hardenbol P, Yu F, Belmont J, Mackenzie J, Bruckner C, Brundage T, Boudreau A, Chow S, Eberle J, Erbilgin A, Falkowski M, Fitzgerald R, Ghose S, Iartchouk O, Jain M, Karlin-Neumann G, Lu X, Miao X, Moore B, Moorhead M, Namsaraev E, Pasternak S, Prakash E, Tran K, Wang Z, Jones HB, Davis RW, Willis TD, Gibbs RA. Highly multiplexed molecular inversion probe genotyping: over 10,000 targeted SNPs genotyped in a single tube assay. Genome Res 2005; 15: 269-275 https://doi.org/10.1101/gr.3185605
  51. Steemers FJ, Gunderson KL. Whole genome genotyping technologies on the BeadArray platform. Biotechnol J 2007; 2: 41-49 https://doi.org/10.1002/biot.200600213
  52. Hagiwara H, Sawakami-Kobayashi K, Yamamoto M, Iwasaki S, Sugiura M, Abe H, Kunihiro-Ohashi S, Takase K, Yamane N, Kato K, Son R, Nakamura M, Segawa O, Yoshida M, Yohda M, Tajima H, Kobori M, Takahama Y, Itakura M, Machida M. Development of an automated SNP analysis method using a paramagnetic beads handling robot. Biotechnol Bioeng 2007; 98: 420-428 https://doi.org/10.1002/bit.21380
  53. Jiang H, Yi M, Mu J, Zhang L, Ivens A, Klimczak LJ, Huyen Y, Stephens RM, Su XZ. Detection of genome wide polymorphisms in the AT rich Plasmodium falciparum genome using a high density microarray. BMC Genomics 2008; 9: 398 https://doi.org/10.1186/1471-2164-9-393
  54. Ribacke U, Mok BW, Wirta V, Normark J, Lundeberg J, Kironde F, Egwang TG, Nilsson P, Wahlgren M. Genome wide gene amplifications and deletions in Plasmodium falciparum. Mol Biochem Parasitol 2007; 155: 33-44 https://doi.org/10.1016/j.molbiopara.2007.05.005
  55. Mourier T, Carret C, Kyes S, Christodoulou Z, Gardner PP, Jeffares DC, Pinches R, Barrell B, Berriman M, Griffiths-Jones S, Ivens A, Newbold C, Pain A. Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res 2008; 18: 281-292 https://doi.org/10.1101/gr.6836108
  56. Foote SJ, Kyle DE, Martin RK, Oduola AM, Forsyth K, Kemp DJ, Cowman AF. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature 1990; 345: 255-258 https://doi.org/10.1038/345255a0
  57. Cowman AF, Galatis D, Thompson JK. Selection for mefloquine resistance in Plasmodium falciparum is linked to amplification of the pfmdr1 gene and cross-resistance to halofantrine and quinine. Proc Natl Acad Sci USA 1994; 9: 1143-1147
  58. Price RN, Uhlemann AC, Brockman A, McGready R, Ashley E, Phaipun L, Patel R, Laing K, Looareesuwan S, White NJ, Nosten F, Krishna S. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 2004; 364: 438-447 https://doi.org/10.1016/S0140-6736(04)16767-6
  59. 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 https://doi.org/10.1093/molbev/msl185
  60. Jiang H, Patel JJ, Yi M, Mu J, Ding J, Stephens R, Cooper RA, Ferdig MT, Su XZ. Genome-wide compensatory changes accompany drug-selected mutations in the Plasmodium falciparum crt gene. PLoS ONE 2008; 3: e2484 https://doi.org/10.1371/journal.pone.0002484
  61. Hardenbol P, Baner J, Jain M, Nilsson M, Namsaraev EA, Karlin-Neumann GA, Fakhrai-Rad H, Ronaghi M, Willis TD, Landegren U, Davis RW. Multiplexed genotyping with sequence-tagged molecular inversion probes. Nat Biotechnol 2003; 21: 673-678 https://doi.org/10.1038/nbt821
  62. Walliker D, Carter R, Morgan S. Genetic recombination in malaria parasites. Nature 1971; 232: 561-562 https://doi.org/10.1038/232561a0
  63. Walliker D, Carter R, Morgan S. Genetic recombination in Plasmodium berghei. Parasitology 1973; 66: 309-320 https://doi.org/10.1017/S0031182000045248
  64. Walliker D, Carter R, Sanderson A. Genetic studies on Plasmodium chabaudi: recombination between enzyme markers. Parasitology 1975; 70: 19-24 https://doi.org/10.1017/S0031182000048824
  65. Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, Lambert L, Furuya T, Bouttenot R, Doll M, Nawaz F, Mu J, Jiang L, Miller LH, Wellems TE. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 2008; 4: 40-51 https://doi.org/10.1016/j.chom.2008.06.001
  66. Wellems TE, Walker-Jonah A, Panton LJ. Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proc Natl Acad Sci USA 1991; 88: 3382-3386 https://doi.org/10.1073/pnas.88.8.3382
  67. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naude B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 2000; 6: 861-871 https://doi.org/10.1016/S1097-2765(05)00077-8
  68. Hayton K, Su XZ. Drug resistance and genetic mapping in Plasmodium falciparum. Curr Genet 2008; 54: 223-239 https://doi.org/10.1007/s00294-008-0214-x
  69. Wang P, Read M, Sims PF, Hyde JE. Sulfadoxine resistance in the human malaria parasite Plasmodium falciparum is determined by mutations in dihydropteroate synthetase and an additional factor associated with folate utilization. Mol Microbiol 1997; 23: 979-986 https://doi.org/10.1046/j.1365-2958.1997.2821646.x
  70. Su XZ, Wootton JC. Genetic mapping in the human malaria parasite Plasmodium falciparum. Mol Microbiol 2004; 53: 1573-1582 https://doi.org/10.1111/j.1365-2958.2004.04270.x
  71. Ferdig MT, Cooper RA, Mu J, Deng B, Joy DA, Su XZ, Wellems TE. Dissecting the loci of low-level quinine resistance in malaria parasites. Mol Microbiol 2004; 52: 985-997 https://doi.org/10.1111/j.1365-2958.2004.04035.x
  72. Hunt P, Cravo PV, Donleavy P, Carlton JM, Walliker D. Chloroquine resistance in Plasmodium chabaudi: are chloroquine-resistance transporter (crt) and multi-drug resistance (mdr1) orthologues involved? Mol Biochem Parasitol 2004; 133: 27-35 https://doi.org/10.1016/j.molbiopara.2003.08.010
  73. Carlton J, Mackinnon M, Walliker D. A chloroquine resistance locus in the rodent malaria parasite Plasmodium chabaudi. Mol Biochem Parasitol 1998; 93: 57-72 https://doi.org/10.1016/S0166-6851(98)00021-8
  74. Cravo PV, Carlton JM, Hunt P, Bisoni L, Padua RA, Walliker D. Genetics of mefloquine resistance in the rodent malaria parasite Plasmodium chabaudi. Antimicrob Agents Chemother 2003; 47: 709-718 https://doi.org/10.1128/AAC.47.2.709-718.2003
  75. Culleton R, Martinelli A, Hunt P, Carter R. Linkage group selection: rapid gene discovery in malaria parasites. Genome Res 2005; 15: 92-97 https://doi.org/10.1101/gr.2866205
  76. Walliker D. Genetic factors in malaria parasites and their effect on host-parasite relationships. In Taylor AE, Muller R eds, Genetic Aspects of Host-Parasite Relationships. Oxford, UK. Blackwell. 1976, p 25-44
  77. Martinelli A, Cheesman S, Hunt P, Culleton R, Raza A, Mackinnon M, Carter R. A genetic approach to the de novo identification of targets of strain-specific immunity in malaria parasites. Proc Natl Acad Sci USA 2005; 102: 814-819 https://doi.org/10.1073/pnas.0405097102
  78. Vaidya AB, Muratova O, Guinet F, Keister D, Wellems TE, Kaslow DC. A genetic locus on Plasmodium falciparum chromosome 12 linked to a defect in mosquito-infectivity and male gametogenesis. Mol Biochem Parasitol 1995; 69: 65-71 https://doi.org/10.1016/0166-6851(94)00199-W
  79. Furuya T, Mu J, Hayton K, Liu A, Duan J, Nkrumah L, Joy DA, Fidock DA, Fujioka H, Vaidya AB, Wellems TE, Su XZ. Disruption of a Plasmodium falciparum gene linked to male sexual development causes early arrest in gametocytogenesis. Proc Natl Acad Sci USA 2005; 102: 16813-16818 https://doi.org/10.1073/pnas.0501858102
  80. Klotz FW, Chulay JD, Daniel W, Miller LH. Invasion of mouse erythrocytes by the human malaria parasite, Plasmodium falciparum. J Exp Med 1987; 165: 1713-1718 https://doi.org/10.1084/jem.165.6.1713
  81. Mackinnon MJ, Gaffney DJ, Read AF. Virulence in rodent malaria: host genotype by parasite genotype interactions. Infect Genet Evol 2002; 1: 287-296 https://doi.org/10.1016/S1567-1348(02)00039-4
  82. Rathod PK, McErlean T, Lee PC. Variations in frequencies of drug resistance in Plasmodium falciparum. Proc Natl Acad Sci USA 1997; 94: 9389-9393 https://doi.org/10.1073/pnas.94.17.9389
  83. Gonzales JM, Patel JJ, Ponmee N, Jiang L, Tan A, Maher SP, Wuchty S, Rathod PK, Ferdig MT. Regulatory hotspots in the malaria parasite genome dictate transcriptional variation. PLoS Biol 2008; 6: e238 https://doi.org/10.1371/journal.pbio.0060238
  84. Lee SA, Yeka A, Nsobya SL, Dokomajilar C, Rosenthal PJ, Talisuna A, Dorsey G. Complexity of Plasmodium falciparum infections and antimalarial drug efficacy at 7 sites in Uganda. J Infect Dis 2006; 193: 1160-1163 https://doi.org/10.1086/501473
  85. Kobbe R, Neuhoff R, Marks F, Adjei S, Langefeld I, von Reden C, Adjei O, Meyer CG, May J. Seasonal variation and high multiplicity of first Plasmodium falciparum infections in children from a holoendemic area in Ghana, West Africa. Trop Med Int Health 2006; 11: 613-619 https://doi.org/10.1111/j.1365-3156.2006.01618.x
  86. 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 https://doi.org/10.1093/molbev/msg162
  87. Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, Chandramohan D, Sharp B. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 2003; 361: 1174-1181 https://doi.org/10.1016/S0140-6736(03)12951-0
  88. McCollum AM, Poe AC, Hamel M, Huber C, Zhou Z, Shi YP, Ouma P, Vulule J, Bloland P, Slutsker L, Barnwell JW, Udhayakumar V, Escalante AA. Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis 2006; 194: 189-197 https://doi.org/10.1086/504687
  89. McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA. Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine-pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother 2007; 51: 2085-2091 https://doi.org/10.1128/AAC.01228-06
  90. Liu S, Mu J, Jiang H, Su XZ. Effects of Plasmodium falciparummixed infections on in vitro antimalarial drug tests and genotyping. Am J Trop Med Hyg 2008; 79: 178-184
  91. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 2004; 5: 557-572 https://doi.org/10.1093/biostatistics/kxh008

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