Skip to main content

Advertisement

Log in

Genetic Distance in Housekeeping Genes Between Plasmodium falciparum and Plasmodium reichenowi and Within P. falciparum

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The time to the most recent common ancestor of the extant populations of Plasmodium falciparum is controversial. The controversy primarily stems from the limited availability of sequences from Plasmodium reichenowi, a chimpanzee malaria parasite closely related to P. falciparum. Since the rate of nucleotide substitution differs in different loci and DNA regions, the estimation of genetic distance between P. falciparum and P. reichenowi should be performed using orthologous sequences that are evolving neutrally. Here, we obtained full-length sequences of two housekeeping genes, sarcoplasmic and endoplasmic reticulum Ca2+-ATPase (serca) and lactate dehydrogenase (ldh), from 11 isolates of P. falciparum and 1 isolate of P. reichenowi and estimate the interspecific genetic distance (divergence) between the two species and intraspecific genetic distance (polymorphism) within P. falciparum. Interspecific distance and intraspecific distance at synonymous sites of interspecies-conserved regions of serca and ldh were 0.0672 ± 0.0088 and 0.0011 ± 0.0007, respectively, using the Nei and Gojobori method. Based on the ratio of interspecific distance to intraspecific distance, the time to the most recent common ancestor of P. falciparum was estimated to be (8.30 ± 5.40) × 104 and (11.62 ± 7.56) × 104 years ago, assuming the divergence time of the two parasite species to be 5 and 7 million years ago, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  • AE Barry A Leliwa M Choi KM Nielsen DL Hartl KP Day (2003) ArticleTitleDNA sequence artifacts and the estimation of time to the most recent common ancestor (TMRCA) of Plasmodium falciparum Mol Biochem Parasitol 130 143–147

    Google Scholar 

  • DJ Conway C Roper AMI Oduola DE Arnot PG Kremsner MP Grobusch C Curtis BM Greenwood (1999) ArticleTitleHigh recombination rate in natural populations of Plasmodium falciparum Proc Natl Acad Sci USA 96 4506–4511

    Google Scholar 

  • U Eckstein-Ludwig RJ Webb IDA van Goethem JM East AG Lee M Kimura PM O’Neil PG Bray SA Ward S Krishna (2003) ArticleTitleArtemisinins target the SERCA of Plasmodium falciparum Nature 424 957–961

    Google Scholar 

  • AA Escalante FJ Ayala (1994) ArticleTitlePhylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences Proc Natl Acad Sci USA 91 11373–11377

    Google Scholar 

  • AA Escalante DE Freeland WE Collins AA Lal (1998a) ArticleTitleThe evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome Proc Natl Acad Sci USA 95 8124–8129

    Google Scholar 

  • AA Escalante AA Lal FJ Ayala (1998b) ArticleTitleGenetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum Genetics 149 189–202

    Google Scholar 

  • MJ Gardner N Hall E Fung O White M Berriman RW Hyman JM Carlton A Pain KE Nelson S Bowman IT Paulsen K James JA Eisen K Rutherford SL Salzberg A Craig S Kyes MS Chan V Nene SJ Shallom B Suh J Peterson S Angiuoli M Pertea J Allen J Selengut D Haft MW Mather AB Vaidya DM Martin AH Fairlamb MJ Fraunholz DS Roos SA Ralph GI McFadden LM Cummings GM Subramanian C Mungall JC Venter DJ Carucci SL Hoffman C Newbold RW Davis CM Fraser B Barrell (2002) ArticleTitleGenome sequence of the human malaria parasite Plasmodium falciparum Nature 419 498–511 Occurrence Handle10.1038/nature01097 Occurrence Handle1:CAS:528:DC%2BD38XnsFais7Y%3D Occurrence Handle12368864

    Article  CAS  PubMed  Google Scholar 

  • AL Hughes (1992) ArticleTitlePositive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum Mol Biol Evol 9 381–393

    Google Scholar 

  • MK Hughes AL Hughes (1995) ArticleTitleNatural selection on Plasmodium surface proteins Mol Biochem Parasitol 71 99–113

    Google Scholar 

  • AL Hughes M Nei (1988) ArticleTitlePattern of nucleotide substitution at MHC class I loci reveals overdominant selection Nature 335 167–170 Occurrence Handle10.1038/335167a0 Occurrence Handle1:CAS:528:DyaL1cXlvVCktrY%3D Occurrence Handle3412472

    Article  CAS  PubMed  Google Scholar 

  • AL Hughes F Verra (2001) ArticleTitleVery large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum Proc R Soc Lond B 268 1855–1860

    Google Scholar 

  • S Jongwutiwes C Putaporntip R Friedman AL Hughes (2002) ArticleTitleThe extent of nucleotide polymorphism is highly variable across a 3-kb region on Plasmodium falciparum chromosome 2 Mol Biol Evol 9 1585–1590

    Google Scholar 

  • DA Joy X Feng J Mu T Furuya K Chotivanich A Krettli M Ho A Wang NJ White E Suh P Beerli X-Z Su (2003) ArticleTitleEarly origin and recent expansion of Plasmodium falciparum Science 300 318–321

    Google Scholar 

  • TH Jukes CR Cantor (1969) Evolution of protein molecules HN Munro (Eds) Mammalian protein metabolism Academic Press New York 21–132

    Google Scholar 

  • O Kaneko M Kimura F Kawamoto MU Ferreira K Tanabe (1997) ArticleTitlePlasmodium falciparum: allelic variation in the merozoite surface protein 1 gene in wild isolates from southern Vietnam Exp Parasitol 86 45–57

    Google Scholar 

  • M Kimura Y Yamaguchi S Takada K Tanabe (1993) ArticleTitleCloning of a Ca2+-ATPase gene of Plasmodium falciparum and comparison with vertebrate Ca2+-ATPase J Cell Sci 104 1129–1136

    Google Scholar 

  • S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular evolutionary genetics analysis software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    Article  CAS  PubMed  Google Scholar 

  • AA Lal IF Goldman (1991) ArticleTitleCircumsporozoite protein gene from Plasmodium reichenowi, a chimpanzee malaria parasite evolutionarily related to the human malaria parasite Plasmodium falciparum J Biol Chem 266 6686–6689

    Google Scholar 

  • DH MacLennan WJ Rice NM Green (1997) ArticleTitleThe mechanism of Ca2+ transport by saro(endo)plasmic reticulum Ca2+-ATPases J Biol Chem 272 28815–28818

    Google Scholar 

  • JH McDonald M Kreitman (1991) ArticleTitleAdaptive protein evolution at the Adh locus in Drosophila Nature 351 652–654 Occurrence Handle10.1038/351652a0 Occurrence Handle1:CAS:528:DyaK3MXks1yrtLs%3D Occurrence Handle1904993

    Article  CAS  PubMed  Google Scholar 

  • L Molineaux (1988) The epidemiology of human malaria as an explanation of its distribution, including some implications for its control WH Wernsdorfer I McGregor (Eds) Malaria: Principles and practice of malariology, Vol 2 Churchill Livingstone Edinburgh 913–998

    Google Scholar 

  • J Mu J Duan KD Makova DA Joy CQ Huynh OH Branch W-H Li X-Z Su (2002) ArticleTitleChromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum Nature 418 323–326

    Google Scholar 

  • M Nei T Gojobori (1986) ArticleTitleSimple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions Mol Biol Evol 3 418–426 Occurrence Handle1:CAS:528:DyaL28Xmt1aisbs%3D Occurrence Handle3444411

    CAS  PubMed  Google Scholar 

  • SM Rich MC Licht RR Hudson FJ Ayala (1998) ArticleTitleMalaria’s Eve: Evidence of a recent population bottleneck throughout the world population of Plasmodium falciparum Proc Natl Acad Sci USA 95 4425–4430

    Google Scholar 

  • J Rozas R Rozas (1999) ArticleTitleDNASP version 3: An integrated program for molecular population genetics and molecular evolution analysis Bioinformatics 15 174–175 Occurrence Handle10.1093/bioinformatics/15.2.174 Occurrence Handle1:CAS:528:DyaK1MXisVOksrY%3D Occurrence Handle10089204

    Article  CAS  PubMed  Google Scholar 

  • N Sakihama T Mitamura A Kaneko T Horii K Tanabe (2001) ArticleTitleLong PCR amplification of Plasmodium falciparum DNA extracted from filter paper blots Exp Parasitol 97 50–54

    Google Scholar 

  • X-Z Su M Ferdig Y Huang CQ Huynh A Lu J You JC Wootton TE Wellems (1999) ArticleTitleA genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum Science 286 1351–1353

    Google Scholar 

  • F Tajima (1989) ArticleTitleStatistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 585–595 Occurrence Handle1:CAS:528:DyaK3cXhslentA%3D%3D Occurrence Handle2513255

    CAS  PubMed  Google Scholar 

  • A Templeton (2002) ArticleTitleOut of Africa again and again Nature 416 45–51

    Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmigin DG Higgins (1997) ArticleTitleThe CLUSTALX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 25 4876–4882 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    Article  CAS  PubMed  Google Scholar 

  • SK Volkman AE Barry EJ Lyons KM Nielsen SM Thomas M Choi SS Thakore KP Day DF Wirth DL Hartl (2001) ArticleTitleRecent origin of Plasmodium falciparum from a single progenitor Science 293 482–484

    Google Scholar 

Download references

Acknowledgments

We thank Dr. T. Mitamura for DNA of the P. falciparum Dd2 strain. This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas from the Japanese Ministry of Education, Culture, Sports, Science and Technology (No. 14021125) and a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (No. 15590377). A. Escalante is supported by a grant from NIH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazuyuki Tanabe.

Additional information

Reviewing Editor: Dr. Martin Kreitman

Appendix

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tanabe, K., Sakihama, N., Hattori, T. et al. Genetic Distance in Housekeeping Genes Between Plasmodium falciparum and Plasmodium reichenowi and Within P. falciparum. J Mol Evol 59, 687–694 (2004). https://doi.org/10.1007/s00239-004-2662-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-2662-3

Keywords

Navigation