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Single nucleotide polymorphisms, putatively neutral DNA markers and population genetic parameters in Indian Plasmodium vivax isolates

Published online by Cambridge University Press:  01 July 2010

BHAVNA GUPTA ,
ADITYA P. DASH ,
NALINI SHRIVASTAVA  and
APARUP DAS
BHAVNA GUPTA
Affiliation:
Evolutionary Genomics and Bioinformatics Laboratory, Division of Genomics and Bioinformatics, National Institute of Malaria Research, Sector-8, Dwarka, New Delhi, 110077, India
ADITYA P. DASH
Affiliation:
World Health Organization, Southeast Asian Regional Office, New Delhi, India
NALINI SHRIVASTAVA
Affiliation:
School of Studies in Biotechnology, Jiwaji University, Gwalior, Madhya Pradesh, India
APARUP DAS*
Affiliation:
Evolutionary Genomics and Bioinformatics Laboratory, Division of Genomics and Bioinformatics, National Institute of Malaria Research, Sector-8, Dwarka, New Delhi, 110077, India
*
*Corresponding author: Evolutionary Genomics and Bioinformatics Laboratory, Division of Genomics and Bioinformatics, National Institute of Malaria Research, Sector-8, Dwarka, New Delhi, 110077, India. Tel: +91 11 25307322. Fax: +91 11 25307 377. E-mail: [email protected]
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Summary

With a view to developing putatively neutral markers based on Single Nucleotide Polymorphisms (SNPs) in the human malaria parasite, Plasmodium vivax, we utilized the published whole genome sequence information of P. falciparum and P. vivax to find a ~200 kb conserved syntenic region between these two species. We have selected 27 non-coding DNA fragments (in introns and intergenic regions) of variable length (300–750 bp) in P. vivax in this syntenic region. PCR of P. vivax isolates of a population sample from India could successfully amplify 17 fragments. Subsequently, DNA sequencing and sequence analysis confirmed the polymorphic status of only 11 fragments. Altogether, 18 SNPs were detected and 2 different measures of nucleotide diversity showed variable patterns across different fragments; in general, introns were less variable than the intergenic regions. All 11 polymorphic fragments were found to be evolving according to a neutral equilibrium model and thus could be utilized as putatively neutral markers for population genetic studies in P. vivax. Different molecular population genetics parameters were also estimated, providing initial insight into the population genetics of Indian P. vivax.

Keywords

malariaIndiaPlasmodium vivaxneutral markerssingle nucleotide polymorphismsevolution
Type
Research Article
Information
Parasitology , Volume 137 , Issue 12 , October 2010 , pp. 1721 - 1730
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Agapow, P. M. and Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes 1, 101–102.CrossRefGoogle Scholar
Andolfatto, P. and Przeworski, M. (2001). Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158, 657–665.CrossRefGoogle ScholarPubMed
Baines, J. F., Das, A., Mousset, S. and Stephan, W. (2004). The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae. Genetics 168, 1987–1998.CrossRefGoogle ScholarPubMed
Barrett, J. C., Fry, B., Maller, J. and Daly, M. J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265.CrossRefGoogle ScholarPubMed
Begun, D. J. and Aquadro, C. F. (1992). Levels of naturally occurring DNA polymorphisms correlate with recombination rates in D. melanogaster. Nature, London 356, 519–520.CrossRefGoogle ScholarPubMed
Braverman, J. M., Hudson, R. R., Kaplan, N. L., Langley, C. H. and Stephan, W. (1995). The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140, 783–796.CrossRefGoogle ScholarPubMed
Brown, A. H. D., Feldman, M. W. and Nevo, E. (1980). Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96, 523–536.CrossRefGoogle ScholarPubMed
Carlton, J. M., Adams, J. H., Silva, J. C., Bidwell, S. L., Lorenzi, H., Caler, E., Crabtree, J., Anginoli, S. V., Merino, E. F., Amedeo, P., Cheng, Q., Conlson, R. M. R., Crabb, B. S., del Po, H. A., Essien, K., Feldblyum, T. V., Fernandez-Becerra, C., Gilson, P. R., Gueye, A. H., Guo Kang'a, S., Kooij, T. W. A., Korsinczky, M., Meyer, E. V.-S., Nene, V., Paulsen, I., White, O., Ralph, S. A., Ren, Q. and Sargeant, T. J. (2008 a). Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455, 757–763.CrossRefGoogle ScholarPubMed
Carlton, J. M., Escalante, A. A., Neafsey, D. and Volkman, S. K. (2008 b). Comparative evolutionary genomics of human malaria parasites. Trends in Parasitology 24, 545–550.CrossRefGoogle ScholarPubMed
Cereb, N., Hughes, A. L. and Yang, S. Y. (1997). Locus-specific conservation of the HLA class I introns by intra-locus homogenization. Immunogenetics 47, 30–36.CrossRefGoogle Scholar
Cole-Tobian, J. and King, C. L. (2003). Diversity and natural selection in Plasmodium vivax Duffy binding protein gene. Molecular and Biochemical Parasitology 127, 121–132.CrossRefGoogle ScholarPubMed
Coombs, G. H., Goldberg, D. E., Klemba, M., Berry, C., Kay, J. and Mottram, J. C. (2001). Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets. Trends in Parasitology 17, 532–537.CrossRefGoogle ScholarPubMed
Cornejo, O. E. and Escalante, A. A. (2000). The origin and age of Plasmodium vivax. Trends in Parasitology 22, 558–563.CrossRefGoogle Scholar
Cui, L., Escalante, A. A., Imwong, M. and Snounou, G. (2003). The genetic diversity of Plasmodium vivax populations. Trends in Parasitology 19, 220–226.CrossRefGoogle ScholarPubMed
Das, A., Mohanty, S. and Stephan, W. (2004). Inferring the population structure and demography of Drosophila ananassae from multilocus data. Genetics 168, 1975–1985.CrossRefGoogle ScholarPubMed
Das, A., Sharma, M., Gupta, B. and Dash, A. P. (2009). Plasmodium falciparum and P. vivax: so similar, yet very different. Parasitology Research 105, 1169–1171.CrossRefGoogle Scholar
Fedorova, L. and Fedorov, A. (2003). Introns in gene evolution. Genetica 118, 123–131.CrossRefGoogle ScholarPubMed
Feng, X., Carlton, J. M., Joy, D. A., Mu, J., Furuya, T., Suh, B. B., Wang, Y., Barnwell, J. W. and Su, X-Z. (2003). Single-nucleotide polymorphisms and genome diversity in Plasmodium vivax. Proceedings of the National Academy of Sciences, USA 100, 8502–8507.CrossRefGoogle ScholarPubMed
Figtree, M., Pasay, C. J., Slade, R., Cheng, Q., Cloonan, N., Walker, J. and Saul, A. (2000). Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA1 and MSP1 genes. Molecular and Biochemical Parasitology 108, 53–66.CrossRefGoogle Scholar
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Fu, Y. X. and Li, W. H. (1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709.CrossRefGoogle ScholarPubMed
Grynberg, P., Fontes, C. J. F., Hughes, A. L. and Braga, E. M. (2008). Polymorphism at the apical membrane antigen 1 locus reflects the world population history of Plasmodium vivax. BMC Evolutionary Biology 8, 123. doi:10.1186/1471-2148-8-123CrossRefGoogle ScholarPubMed
Haubold, B., Travisano, M., Rainey, P. B. and Hudson, R. R. (1998). Detecting linkage disequilibrium in bacterial populations. Genetics 150, 1341–1348.CrossRefGoogle ScholarPubMed
Hawkins, V. N., Auliff, A., Prajapati, S. K., Rungsihirunrat, K., Hapuarachchi, H. C., Maestre, A., O'Neil, M. T., Cheng, Q., Joshi, H., Na-Bangchang, K. and Sibley, C. H. (2008). Multiple origins of resistance-conferring mutations in Plasmodium vivax dihydrofolate reductase. Malaria Journal 7, 72. doi:10.1186/1475-2875-7-72CrossRefGoogle ScholarPubMed
Hudson, R. R. (1987). Estimating the recombination parameter of a finite population model without selection. Genetics Research Cambridge 50, 245–250.CrossRefGoogle ScholarPubMed
Hughes, A. L. (2000). Evolution of introns and exons of class II MHC genes of vertebrates. Immunogenetics 51, 473–486.CrossRefGoogle ScholarPubMed
Imwong, M., Nair, S., Pukrittayakamee, S., Sudimack, D., Williams, J. T., Mayxay, M., Newton, P. N., Jung, R. K., Nandy, A., Osorio, L., Carlton, J. M., White, N. J., Day, N. P. J. and Anderson, T. J. C. (2007) Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. International Journal for Parasitology 37, 1013–1022.CrossRefGoogle ScholarPubMed
Imwong, M., Pukrittayakamee, S., Cheng, Q., Moore, C., Looareesuwan, S., Snounou, G., White, N. J. and Day, N. P. J. (2005). Limited polymorphism in the dihydropteroate synthetase gene (dhps) of Plasmodium vivax isolates from Thailand. Antimicrobial Agents and Chemotherapy 49, 4393–4395.CrossRefGoogle ScholarPubMed
Johnston, S. P., Pieniazek, N. J., Xayavong, M. V., Slemenda, S. B., Wilkins, P. P. and da Silva, A. J. (2006). PCR as a confirmatory technique for laboratory diagnosis of malaria. Journal of Clinical Microbiology 44, 1087–1089.CrossRefGoogle ScholarPubMed
Jongwutiwes, S., Putaporntip, C., Iwasaki, T., Ferreira, M. U., Kanbara, H. and Hughes, A. L. (2005). Mitochondrial genome sequences support ancient population expansion in Plasmodium vivax. Molecular Biology and Evolution 22, 1733–1739.CrossRefGoogle ScholarPubMed
Jongwutiwes, S., Putaporntip, C., Friedman, R. and Hughes, A. L. (2002). The extent of nucleotide polymorphism is highly variable across a 3-kb region on Plasmodium falciparum chromosome 2. Molecular Biology and Evolution 19, 1585–1590.CrossRefGoogle ScholarPubMed
Joshi, H., Valecha, N., Verma, A., Kaul, A., Mallick, P. K., Shalini, S., Prajapati, S. K., Sharma, S. K., Dev, V., Biswas, S., Nanda, N., Malhotra, M. S., Subbarao, S. K. and Dash, A. P. (2007). Genetic structure of Plasmodium falciparum field isolates in eastern and north-eastern India. Malaria Journal 6, 60. doi:10.1186/1475-2875-6-60CrossRefGoogle ScholarPubMed
Joshi, H., Subbarao, S. K., Adak, T., Nanda, N., Ghosh, S. K., Carter, R. and Sharma, V. P. (1997). Genetic structure of Plasmodium vivax isolates in India. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 231–235.CrossRefGoogle ScholarPubMed
Joshi, H., Subbarao, S. K., Raghavendra, K. and Sharma, V. P. (1989). Plasmodium vivax: enzyme polymorphism in isolates of Indian origin. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 179–181.CrossRefGoogle ScholarPubMed
Joy, D. A., Gonzalez-Ceron, L., Carlton, J. M., Gueye, A., Fay, M., McCutchan, T. F. and Su, X-Z. (2008). Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Molecular Biology and Evolution 25, 1245–1252.CrossRefGoogle ScholarPubMed
Kim, J. R., Imwong, M., Nandy, A., Chotivanich, K., Nontprasert, A., Tonomsing, N., Maji, A., Addy, M., Day, N. P. J., White, N. and Pukrittayakamee, S. (2006). Genetic diversity of Plasmodium vivax in Kolkata, India. Malaria Journal 5, 71. doi:10.1186/1475-2875-5-71CrossRefGoogle ScholarPubMed
Leclerc, M. C., Durand, P., Gauthier, C., Patot, S., Billotte, N., Menegon, M., Severini, C., Ayala, F. J. and Renaud, F. (2004). Meager genetic variability of the human malaria agent Plasmodium vivax. Proceedings of the National Academy of Sciences, USA 101, 14455–14460.CrossRefGoogle ScholarPubMed
Leclerc, M. C., Gauthier, C., Villegas, L. and Urdaneta, L. (2005). Genetic diversity of merozoite surface protein-1 gene of Plasmodium vivax isolates in mining villages of Venezuela (Bolivar State). Acta Tropica 95, 26–32.CrossRefGoogle ScholarPubMed
Lim, C. S., Tazi, L. and Ayala, F. J. (2005). Plasmodium vivax: recent world expansion and genetic identity to Plasmodium simium. Proceedings of the National Academy of Sciences, USA 102, 15523–15528.CrossRefGoogle ScholarPubMed
Mu, J., Joy, D. A., Duan, J., Huang, Y., Carlton, J., Walker, J., Barnwell, J., Beerli, P., Charleston, M. A., Pybus, O. G. and Su, X. Z. (2005). Host switches leads to emergence of Plasmodium vivax malaria in humans. Molecular Biology and Evolution 22, 1686–1693.CrossRefGoogle ScholarPubMed
Na, B-K., Lee, E-G., Lee, H-W., Cho, S-H., Bae, Y-A., Kong, Y., Lee, J-K. and Kim, T-S. (2004). Aspartic proteases of Plasmodium vivax are highly conserved in wild isolates. Korean Journal of Parasitology 42, 61–66.CrossRefGoogle ScholarPubMed
Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press, New York, USA.CrossRefGoogle Scholar
Parsch, J. (2003). Selective constraint on intron evolution in Drosophila. Genetics 165, 1843–1851.CrossRefGoogle ScholarPubMed
Prajapati, S. K., Verma, A., Adak, T., Yadav, R. S., Kumar, A., Eapen, A., Das, M. K., Singh, N., Sharma, S. K., Rizvi, M. A., Dash, A. P. and Joshi, H. (2006). Allelic dimorphism of Plasmodium vivax gam-1 in the Indian subcontinent. Malaria Journal 5, 90. doi:10.1186/1475-2875-5-90.CrossRefGoogle ScholarPubMed
Rajesh, V., Elamaran, M., Vidya, S., Gowrishankar, M., Kochar, D. and Das, A. (2007). Plasmodium vivax: genetic diversity of the apical membrane antigen-1 (AMA-1) in isolates from India. Experimental Parasitology 116, 252–256.CrossRefGoogle ScholarPubMed
Rayner, J. C., Tran, T. M., Corredor, V., Huber, C. S., Barnwell, J. W. and Galinski, M. R. (2005). Dramatic difference in diversity between Plasmodium falciparum and Plasmodium vivax reticulocytes binding-like genes. American Journal of Tropical Medicine and Hygiene 72, 666–674.CrossRefGoogle ScholarPubMed
Rozas, J., Sanchez-DelBarrio, J. C., Messeguer, X. and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle ScholarPubMed
Singh, V., Mishra, N., Awasthi, G., Dash, A. P. and Das, A. (2009). Why is it important to study malaria epidemiology in India? Trends in Parasitology 25, 452–457.CrossRefGoogle ScholarPubMed
Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460.CrossRefGoogle ScholarPubMed
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Thakur, A., Alam, M. T., Bora, H., Kaur, P. and Sharma, Y. D. (2008). Plasmodium vivax: Sequence polymorphism and effect of natural selection at apical membrane antigen 1 (PvAMA1) among Indian population. Gene 419, 35–42.CrossRefGoogle ScholarPubMed
Väli, Ü., Brandström, M., Johansson, M. and Ellegren, H. (2008). Insertion-deletion polymorphisms (indels) as genetic markers in natural populations. BMC Genetics 9, 8. doi:10.1186/1471-2156-9-8.CrossRefGoogle ScholarPubMed
Volkman, S. K., Barry, A. E., Lyons, E. J., Nielsen, K. M., Thomas, S. M., Choi, M., Thakore, S. S., Day, K. P., Wirth, D. F. and Hartl, D. L. (2001). Recent origin of Plasmodium falciparum from a single progenitor. Science 293, 482–484.CrossRefGoogle ScholarPubMed
Watterson, G. (1975). On the number of segregation sites. Theoretical Population Biology 7, 256–276.CrossRefGoogle ScholarPubMed
Weir, B. S. (1996). In Genetic Data Analysis II (ed. Austin, D. F.), pp. 216–216. Sinauer Associates, Sunderland, MA, USA.Google Scholar
World Health Organization (2008). World malaria report. World Health Organization, Geneva, Switzerland.Google Scholar
Zhang, L-B. and Ge, S. (2007). Multilocus analysis of nucleotide variation and speciation in Oryza officinalis and its closer relatives. Molecular Biology and Evolution 24, 769–783.CrossRefGoogle Scholar