Indels, structural variation, and recombination drive genomic diversity in Plasmodium falciparum

Genome Research

Volumn 26, Issue 9, 2016, Pages 1288-1299

  Miles, Alistair ^a,b   Iqbal, Zamin ^c   Vauterin, Paul ^a   Pearson, Richard ^a,b   Campino, Susana ^b   Theron, Michel ^b   Gould, Kelda ^b   Mead, Daniel ^b   Drury, Eleanor ^b   O'Brien, John ^d   Rubio, Valentin Ruano ^e   Macinnis, Bronwyn ^e   Mwangi, Jonathan ^f,g   Samarakoon, Upeka ^h   Ranford Cartwright, Lisa ^g   Ferdig, Michael ^h   Hayton, Karen ⁱ   Su, Xin Zhuan ⁱ   Wellems, Thomas ⁱ   Rayner, Julian ^b   McVean, Gil ^c   Kwiatkowski, Dominic ^a,b   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d BOWDOIN COLLEGE   (United States)

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

^f MOUNT KENYA UNIVERSITY   (Kenya)

^g UNIVERSITY OF GLASGOW   (United Kingdom)

^h UNIVERSITY OF NOTRE DAME   (United States)

ⁱ NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COPY NUMBER VARIATION; DENSITY; DRUG RESISTANCE; GENE SEQUENCE; GENETIC CROSS; GENETIC VARIATION; GENOTYPE; INDEL MUTATION; MEIOTIC RECOMBINATION; MICROBIAL DIVERSITY; MICROBIAL GENOME; NONHUMAN; PARENT; PHENOTYPIC PLASTICITY; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROGENY; SINGLE NUCLEOTIDE POLYMORPHISM; CHROMOSOMAL MAPPING; DRUG EFFECTS; GENETIC RECOMBINATION; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; HUMAN; MALARIA FALCIPARUM; MEIOSIS; PARASITOLOGY; PATHOGENICITY;

CHROMOSOME MAPPING; DNA COPY NUMBER VARIATIONS; DRUG RESISTANCE; GENETIC VARIATION; GENOME, PROTOZOAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INDEL MUTATION; MALARIA, FALCIPARUM; MEIOSIS; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC;

EID: 84984985832     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.203711.115     Document Type: Article

References (79)

1. Anderson TJC, Patel J, Ferdig MT. 2009. Gene copy number and malaria biology. Trends Parasitol 25: 336-343.
2. Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois A-C, Khim N, Kim S, Duru V, Bouchier C, Ma L, et al. 2014. A molecular marker of artemisinin- resistant Plasmodium falciparum malaria. Nature 505: 50-55.
3. Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, et al. 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411-423.
4. Baudat F, de Massy B. 2007. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565-577.
5. Bopp SER, Manary MJ, Bright AT, Johnston GL, Dharia NV, Luna FL, McCormack S, Plouffe D, McNamara CW, Walker JR, et al. 2013. Mitotic evolution of Plasmodium falciparum shows a stable core genome but recombination in antigen families. PLoS Genet 9: E1003293.
6. Brick K, Watanabe J, Pizzi E. 2008. Core promoters are predicted by their distinct physicochemical properties in the genome of Plasmodium falciparum. Genome Biol 9: R178.
7. Cameron AC, Trivedi PK. 1990. Regression-based tests for overdispersion in the Poisson model. J Econom 46: 347-364.
8. Chen J-Q, Wu Y, Yang H, Bergelson J, Kreitman M, Tian D. 2009. Variation in the ratio of nucleotide substitution and indel rates across genomes in mammals and bacteria. Mol Biol Evol 26: 1523-1531.
9. Claessens A, Hamilton WL, Kekre M, Otto TD, Faizullabhoy A, Rayner JC, Kwiatkowski D. 2014. Generation of antigenic diversity in Plasmodium falciparum by structured rearrangement of var genes during mitosis PLoS Genet 10: E1004812.
10. Cowman AF, Galatis D, Thompson JK. 1994. Selection for mefloquine resistance in Plasmodium falciparum is linked to amplification of the pfmdr1gene and cross-resistance to halofantrine and quinine. Proc Natl Acad Sci 91: 1143-1147.
11. Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, WongW, Baro N, Ndiaye D, Fall FB, Ndiop M, et al. 2015. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci 112: 7067-7072.
12. DePristo MA, Zilversmit MM, Hartl DL. 2006. On the abundance, amino acid composition, and evolutionary dynamics of low-complexity regions in proteins. Gene 378: 19-30.
13. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
14. Drouaud J, Camilleri C, Bourguignon P-Y, Canaguier A, Bérard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, et al. 2006. Variation in crossingover rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". Genome Res 16: 106-114.
15. Fang H, Wu Y, Narzisi G, O'Rawe JA, Barrón LTJ, Rosenbaum J, Ronemus M, Iossifov I, Schatz MC, Lyon GJ. 2014. Reducing INDEL calling errors in whole genome and exome sequencing data. Genome Med 6: 89.
16. Ferreira MU, Ribeiro WL, Tonon AP, Kawamoto F, Rich SM. 2003. Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene 304: 65-75.
17. Flueck C, Bartfai R, Volz J, Niederwieser I, Salcedo-Amaya AM, Alako BTF, Ehlgen F, Ralph SA, Cowman AF, Bozdech Z, et al. 2009. Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 5: E1000569.
18. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, Scherf A. 2000. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022.
19. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
20. Gonzales JM, Patel JJ, Ponmee N, Jiang L, Tan A, Maher SP, Wuchty S, Rathod PK, Ferdig MT. 2008. Regulatory hotspots in the malaria parasite genome dictate transcriptional variation. PLoS Biol 6: E238.
21. Gymrek M, Willems T, Guilmatre A, Zeng H, Markus B, Georgiev S, Daly MJ, Price AL, Pritchard JK, Sharp AJ, et al. 2015. Abundant contribution of short tandem repeats to gene expression variation in humans. Nat Genet 48: 22-29.
22. Haerty W, Golding GB. 2011. Increased polymorphism near low-complexity sequences across the genomes of Plasmodium falciparum isolates. Genome Biol Evol 3: 539-550.
23. Hastings PJ. 1992. Mechanism and control of recombination in fungi. Mutat Res 284: 97-110.
24. Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, Lambert L, Furuya T, Bouttenot R, Doll M, et al. 2008. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4: 40-51.
25. Heinberg A, Siu E, Stern C, Lawrence EA, Ferdig MT, Deitsch KW, Kirkman LA. 2013. Direct evidence for the adaptive role of copy number variation on antifolate susceptibility in Plasmodium falciparum. Mol Microbiol 88: 702-712.
26. Hilliker AJ, Harauz G, Reaume AG, Gray M, Clark SH, Chovnick A. 1994. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics 137: 1019-1026.
27. Iqbal Z, Caccamo M, Turner I, Flicek P, McVean G. 2012. De novo assembly and genotyping of variants using colored de Bruijn graphs. Nat Genet 44: 226-232.
28. Jeffares DC, Pain A, Berry A, Cox AV, Stalker J, Ingle CE, Thomas A, Quail MA, Siebenthall K, Uhlemann A-C, et al. 2007. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet 39: 120-125.
29. Jeffreys AJ, May CA. 2004. Intense and highly localized gene conversion activity in human meiotic crossover hot spots. Nat Genet 36: 151-156.
30. Jiang H, Li N, Gopalan V, Zilversmit MM, Varma S, Nagarajan V, Li J, Mu J, Hayton K, Henschen B, et al. 2011. High recombination rates and hotspots in a Plasmodium falciparum genetic cross. Genome Biol 12: R33.
31. Kerr PJ, Ranford-Cartwright LC, Walliker D. 1994. Proof of intragenic recombination in Plasmodium falciparum. Mol Biochem Parasitol 66: 241-248.
32. Kidgell C, Volkman SK, Daily J, Borevitz JO, Plouffe D, Zhou Y, Johnson JR, Le Roch K, Sarr O, Ndir O, et al. 2006. A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog 2: E57.
33. Kleiber C, Zeileis A. 2008. Applied econometrics with R (Use R!). Springer, New York.
34. Kondrashov FA. 2012. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci 279: 5048-5057.
35. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, Turner DJ. 2009. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat Methods 6: 291-295.
36. Lasonder E, Janse CJ, van Gemert G-J, Mair GR, Vermunt AMW, Douradinha BG, van Noort V, Huynen MA, Luty AJF, Kroeze H, et al. 2008. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog 4: E1000195.
37. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754-1760.
38. Li Y-C, Korol AB, Fahima T, Beiles A, Nevo E. 2002. Microsatellites: genomic distribution, putative functions and mutational mechanisms: A review. Mol Ecol 11: 2453-2465.
39. Lovett ST. 2004. Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences. Mol Microbiol 52: 1243-1253.
40. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. 2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
41. Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, O'Brien J, Djimde A, Doumbo O, Zongo I, et al. 2012. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487: 375-379.
42. Martinez-Perez E, Colaiácovo MP. 2009. Distribution of meiotic recombination events: Talking to your neighbors. Curr Opin Genet Dev 19: 105-112.
43. Miller DE, Takeo S, Nandanan K, Paulson A, Gogol MM, Noll AC, Perera AG, Walton KN, Gilliland WD, Li H, et al. 2012. A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster. G3 (Bethesda) 2: 249-260.
44. Miotto O, Almagro-Garcia J, Manske M, Macinnis B, Campino S, Rockett KA, Amaratunga C, Lim P, Suon S, Sreng S, et al. 2013. Multiple populations of artemisinin-resistant Plasmodium falciparum in Cambodia. Nat Genet 45: 648-655.
45. Mira-Martínez S, Rovira-Graells N, Crowley VM, Altenhofen LM, Llinás M, Cortés A. 2013. Epigenetic switches in clag3 genes mediate blasticidin S resistance in malaria parasites. Cell Microbiol 15: 1913-1923.
46. Mok S, Liong K-Y, Lim E-H, Huang X, Zhu L, Preiser PR, Bozdech Z. 2014. Structural polymorphism in the promoter of pfmrp2 confers Plasmodium falciparum tolerance to quinoline drugs. Mol Microbiol 91: 918-934.
47. Montgomery SB, Goode DL, Kvikstad E, Albers CA, Zhang ZD, Mu XJ, Ananda G, Howie B, Karczewski KJ, Smith KS, et al. 2013. The origin, evolution, and functional impact of short insertion-deletion variants identified in 179 human genomes. Genome Res 23: 749-761.
48. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, Seydel K, McVean GA, Su X. 2007. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 39: 126-130.
49. Muralidharan V, Goldberg DE. 2013. Asparagine repeats in Plasmodium falciparum proteins: good for nothing? PLoS Pathog 9: E1003488.
50. Muzzey D, Schwartz K, Weissman JS, Sherlock G. 2013. Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure. Genome Biol 14: R97.
51. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. 2005. A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321-324.
52. Nair S, Nash D, Sudimack D, Jaidee A, Barends M, Uhlemann A-C, Krishna S, Nosten F, Anderson TJC. 2007. Recurrent gene amplification and soft selective sweeps during evolution of multidrug resistance in malaria parasites. Mol Biol Evol 24: 562-573.
53. Nair S, Miller B, Barends M, Jaidee A, Patel J, Mayxay M, Newton P, Nosten F, Ferdig MT, Anderson TJC. 2008. Adaptive copy number evolution in malaria parasites. PLoS Genet 4: E1000243.
54. Nair S, Nkhoma SC, Serre D, Zimmerman PA, Gorena K, Daniel BJ, Nosten F, Anderson TJC, Cheeseman IH. 2014. Single-cell genomics for dissection of complex malaria infections. Genome Res 24: 1028-1038.
55. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA, Lukens A, Rosen D, Daniels R, Houde N, et al. 2008. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol 9: R171.
56. Padhukasahasram B, Rannala B. 2013. Meiotic gene-conversion rate and tract length variation in the human genome. Eur J Hum Genet doi:10.1038/ejhg.2013.30.
57. R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org/.
58. Ranford-Cartwright LC, Mwangi JM. 2012. Analysis of malaria parasite phenotypes using experimental genetic crosses of Plasmodium falciparum. Int J Parasitol 42: 529-534.
59. Robasky K, Lewis NE, Church GM. 2014. The role of replicates for error mitigation in next-generation sequencing. Nat Rev Genet 15: 56-62.
60. Rosenthal PJ. 2013. The interplay between drug resistance and fitness in malaria parasites. Mol Microbiol 89: 1025-1038.
61. Roy SW, Ferreira MU, Hartl DL. 2008. Evolution of allelic dimorphism in malarial surface antigens. Heredity (Edinb) 100: 103-110.
62. Samarakoon U, Gonzales JM, Patel JJ, Tan A, Checkley L, Ferdig MT. 2011a. The landscape of inherited and de novo copy number variants in a Plasmodium falciparum genetic cross. BMC Genomics 12: 457.
63. Samarakoon U, Regier A, Tan A, Desany BA, Collins B, Tan JC, Emrich SJ, Ferdig MT. 2011b. High- Throughput 454 resequencing for allele discovery and recombination mapping in Plasmodium falciparum. BMC Genomics 12: 116.
64. Saunders IW, Brohede J, Hannan GN. 2007. Estimating genotyping error rates from Mendelian errors in SNP array genotypes and their impact on inference. Genomics 90: 291-296.
65. Sepúlveda N, Campino SG, Assefa SA, Sutherland CJ, Pain A, Clark TG. 2013. A Poisson hierarchical modelling approach to detecting copy number variation in sequence coverage data. BMC Genomics 14: 128.
66. Su Xz, Wellems TE. 1996. Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics 33: 430-444.
67. Su X, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, Wootton JC, Wellems TE. 1999. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science 286: 1351-1353.
68. Su X, Hayton K, Wellems TE. 2007. Genetic linkage and association analyses for trait mapping in Plasmodium falciparum. Nat Rev Genet 8: 497-506.
69. Tan JC, Tan A, Checkley L, Honsa CM, Ferdig MT. 2010. Variable numbers of tandem repeats in Plasmodium falciparum genes. J Mol Evol 71: 268-278.
70. Tsai IJ, Burt A, Koufopanou V. 2010. Conservation of recombination hotspots in yeast. Proc Natl Acad Sci 107: 7847-7852.
71. Valli A, López-Moya JJ, García JA. 2007. Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88: 1016-1028.
72. Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, Del Angel G, Levy- Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, et al. 2013. In Current protocols in bioinformatics (ed. Bateman A, et al.). Wiley, Hoboken, NJ.
73. Völker M, Backström N, Skinner BM, Langley EJ, Bunzey SK, Ellegren H, Griffin DK. 2010. Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20: 503-511.
74. Walker-Jonah A, Dolan SA, Gwadz RW, Panton LJ, Wellems TE. 1992. An RFLP map of the Plasmodium falciparum genome, recombination rates and favored linkage groups in a genetic cross. Mol Biochem Parasitol 51: 313-320.
75. Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236: 1661-1666.
76. Wellems TE, Panton LJ, Gluzman IY, do Rosario VE, Gwadz RW, Walker- Jonah A, Krogstad DJ. 1990. Chloroquine resistance not linked to mdrlike genes in a Plasmodium falciparum cross. Nature 345: 253-255.
77. Wellems TE, Walker-Jonah A, Panton LJ. 1991. Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proc Natl Acad Sci 88: 3382-3386.
78. Youds JL, Boulton SJ. 2011. The choice in meiosis-defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501-513.
79. Zilversmit MM, Volkman SK, DePristo MA, Wirth DF, Awadalla P, Hartl DL. 2010. Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Mol Biol Evol 27: 2198-2209.