Genetic Polymorphism and Natural Selection in the Malaria Parasite Plasmodium falciparum

Genetics - Tập 149 Số 1 - Trang 189-202 - 1998
Ananías A. Escalante1, Altaf A. Lal1, Francisco J. Ayala2
1Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Chamblee, Georgia 30341
2Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92697-2525

Tóm tắt

AbstractWe have studied the genetic polymorphism at 10 Plasmodium falciparum loci that are considered potential targets for specific antimalarial vaccines. The polymorphism is unevenly distributed among the loci; loci encoding proteins expressed on the surface of the sporozoite or the merozoite (AMA-1, CSP, LSA-1, MSP-1, MSP-2, and MSP-3) are more polymorphic than those expressed during the sexual stages or inside the parasite (EBA-175, Pfs25, PF48/45, and RAP-1). Comparison of synonymous and nonsynonymous substitutions indicates that natural selection may account for the polymorphism observed at seven of the 10 loci studied. This inference depends on the assumption that synonymous substitutions are neutral, which we test by analyzing codon bias and G+C content in a set of 92 gene loci. We find evidence for an overall trend towards increasing A+T richness, but no evidence for mutation bias. Although the neutrality of synonymous substitutions is not definitely established, this trend towards an A+T rich genome cannot explain the accumulation of substitutions at least in the case of four genes (AMA-1, CSP, LSA-1, and PF48/45) because the G↔C transversions are more frequent than expected. Moreover, the Tajima test manifests positive natural selection for the MSP-1 and, less strongly, MSP-3 polymorphisms; the McDonald-Kreitman test manifests natural selection at LSA-1 and PF48/45. We conclude that there is definite evidence for positive natural selection in the genes encoding AMA-1, CSP, LSA-1, MSP-1, and Pfs48/45. For four other loci, EBA-175, MSP-2, MSP-3, and RAP-1, the evidence is limited. No evidence for natural selection is found for Pfs25.

Từ khóa


Tài liệu tham khảo

Anders, 1994, Candidate antigens for an asexual blood stage vaccine against falciparum malaria, Molecular Immunological Considerations in Malaria Vaccine Development, 169

Andersson, 1996, Codon usage and base composition in Rickettsia prowazekii, J. Mol. Evol., 42, 525, 10.1007/BF02352282

Ayala, 1994, Molecular genetics of speciation and human origins, Proc. Natl. Acad. Sci. USA, 91, 6787, 10.1073/pnas.91.15.6787

Bhattacharya, 1995, Merozoite surface antigen 2 (MSA-2) gene of Plasmodium falciparum strains from India, Mol. Biochem. Parasitol., 74, 125, 10.1016/0166-6851(96)83010-6

Brown, 1982, Mitochondrial DNA sequences of primates: tempo and mode of evolution, J. Mol. Evol., 18, 225, 10.1007/BF01734101

Campbell, 1989, DNA sequence of the gene encoding a Plasmodium falciparum malaria candidate vaccine antigen, Nucleic Acids Res., 17, 5854, 10.1093/nar/17.14.5854

Caspers, 1989, The circumsporozoite protein gene from NF54, a Plasmodium falciparum isolate used in malaria vaccine trials, Mol. Biochem. Parasitol., 35, 185, 10.1016/0166-6851(89)90121-7

Chang, 1988, Plasmodium falciparum: gene structure and hydropathy profile of the major merozoite surface antigen (gp195) of the Uganda-Palo Alto isolate, Exp. Parasitol., 67, 1, 10.1016/0014-4894(88)90002-1

Cheng, 1986, General Parasitology, Ed. 2

Coatney, 1971, The Primate Malarias

Collins, 1993, Plasmodia of nonhuman primates, Parasitic Protozoa, 105, 10.1016/B978-0-12-426015-3.50008-X

Collins, 1994, Rates of transition and transversion in coding sequences since the human-rodent divergence, Genomics, 20, 386, 10.1006/geno.1994.1192

Conover, 1980, Practical Nonparametric Statistics

Conway, 1997, Natural selection on polymorphic malaria antigens and the search for a vaccine, Parasitol. Today, 13, 26, 10.1016/S0169-4758(96)10077-6

Conway, 1991, Plasmodium falciparum: intragenic recombination and nonrandom associations between polymorphic domains of the precursor to the major merozoite surface antigens, Exp. Parasitol., 73, 469, 10.1016/0014-4894(91)90071-4

Crozier, 1993, The mitochondrial genome of the honeybee Apis mellifera complete sequence and genome organization, Genetics, 133, 97, 10.1093/genetics/133.1.97

Dame, 1984, Structure of the gene encoding the immunodominant surfaceantigen on the sporozoite of the human malaria parasite Plasmodium falciparum, Science, 225, 593, 10.1126/science.6204383

del Portillo, 1987, Circumsporozoite gene of a Plasmodium falciparum strain from Thailand, Mol. Biochem. Parasitol., 24, 289, 10.1016/0166-6851(87)90161-7

Dunn, 1961, Multiple comparisons among means, J. Am. Stat. Assoc., 56, 52, 10.1080/01621459.1961.10482090

Efron, 1993, An Introduction to the Bootstrap, 10.1007/978-1-4899-4541-9

Endo, 1996, Large-scale search for genes on which positive selection may operate, Mol. Biol. Evol., 13, 685, 10.1093/oxfordjournals.molbev.a025629

Escalante, 1994, Phylogeny of the malarial genus Plasmodium derived from rRNA gene sequences, Proc. Natl. Acad. Sci. USA, 91, 11373, 10.1073/pnas.91.24.11373

Escalante, 1995, Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene, Mol. Biol. Evol., 12, 616

Escalante, 1997, Phylogenetic study of the genus Plasmodium based on the secondary structure-based alignment of the small subunit ribosomal RNA, Mol. Biochem. Parasitol., 90, 317, 10.1016/S0166-6851(97)00121-7

Fenton, 1991, Structural and antigenic polymorphism of the 35- to 48-kilodalton merozoite surface antigen (MSA-2) of the malaria parasite Plasmodium falciparum, Mol. Cell. Biol., 11, 963

Fidock, 1994, Plasmodium falciparum liver stage antigen-1 is well conserved and contains B and T cell determinants, J. Immunol., 153, 190, 10.4049/jimmunol.153.1.190

Frontali, 1994, Genome plasticity in Plasmodium, Genetica, 94, 91, 10.1007/BF01443424

Gillespie, 1991, The Causes of Molecular Evolution

Gillespie, 1994, Alternatives to Neutral Theory, Non-Neutral Evolution: Theories and Molecular Data, 1, 10.1007/978-1-4615-2383-3_1

Gleason, 1997, Mitochondrial DNA phylogenies for the Drosophila obscura group, Evolution, 51, 433, 10.1111/j.1558-5646.1997.tb02430.x

Gojobori, 1982, Patterns of nucleotide substitutions in pseudogenes and functional genes, J. Mol. Evol., 18, 360, 10.1007/BF01733904

Hamblin, 1997, Contrasting patterns of nucleotide sequence variation at the glucose dehydrogenase (Gld) locus in different populations of Drosophila melanogaster, Genetics, 145, 1053, 10.1093/genetics/145.4.1053

Hancock, 1996, The quest for α: developments in multiple comparison procedures in the quarter century since Games (1971), Rev. Edu. Res., 66, 269

Hartl, 1991, Inference of selection and recombination from nucleotide sequence data, J. Evol. Biol., 4, 519, 10.1046/j.1420-9101.1991.4040519.x

Hill, 1992, Molecular analysis of the association of HLA-B53 and resistance to severe malaria, Nature, 360, 434, 10.1038/360434a0

Huber, 1997, Limited sequence polymorphism in the Plasmodium falciparum merozoite surface antigen 3, Mol. Biochem. Parasitol., 87, 231, 10.1016/S0166-6851(97)00067-4

Hudson, 1993, The how and why of generating gene genealogies, Mechanisms of Molecular Evolution: Introduction to Molecular Paleopopulation Biology, 23

Hudson, 1994, Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster, Genetics, 136, 1329, 10.1093/genetics/136.4.1329

Hughes, 1991, Circumsporozoite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions, Genetics, 127, 345, 10.1093/genetics/127.2.345

Hughes, 1992, Positive selection and intrallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum, Mol. Biol. Evol., 9, 381

Hughes, 1995, Natural selection on Plasmodium surface proteins, Mol. Biochem. Parasitol., 71, 99, 10.1016/0166-6851(95)00037-2

Hughes, 1988, Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection, Nature, 335, 167, 10.1038/335167a0

Hughes, 1989, Nucleotide substitution at major histocompatibility complex class II loci: evidence of overdominant selection, Nature, 335, 167, 10.1038/335167a0

Hyde, 1987, Anomalous dinucleotide frequencies in both coding and non-coding regions from the genome of the human malaria parasite Plasmodium falciparum, Gene, 61, 177, 10.1016/0378-1119(87)90112-0

Ina, 1995, New methods for estimating the numbers of synonymous and nonsynonymous substitutions, J. Mol. Evol., 40, 190, 10.1007/BF00167113

Ina, 1994, Statistical analysis of nucleotide sequences of the hemagglutinin gene of human influenza A viruses, Proc. Natl. Acad. Sci. USA, 91, 8388, 10.1073/pnas.91.18.8388

Inohira, 1997, Nucleotide sequence divergence in the A+T-rich region of mitochondrial DNA in Drosophila simulans and Drosophila mauritiana, Mol. Biol. Evol., 14, 814, 10.1093/oxfordjournals.molbev.a025822

Jongwutiwes, 1993, Sequence conservation in the C-terminal part of the precursor to the major merozoite surface proteins (MSP-1) of Plasmodium falciparum from field isolates, Mol. Biochem. Parasitol., 59, 95, 10.1016/0166-6851(93)90010-U

Jongwutiwes, 1994, Allelic variation in the circumsporozoite protein of Plasmodium falciparum from Thai field isolates, Am. J. Trop. Med. Hyg., 51, 659, 10.4269/ajtmh.1994.51.659

Jukes, 1969, Evolution of protein molecules, Mammalian Protein Metabolism, 21, 10.1016/B978-1-4832-3211-9.50009-7

Kaslow, 1994, Progress toward a transmission-blocking vaccine, Molecular Immunological Considerations in Malaria Vaccine Development, 209

Kaslow, 1989, Minimal variation in a vaccine candidate from the sexual stage of Plasmodium falciparum, Mol. Biochem. Parasitol., 32, 101, 10.1016/0166-6851(89)90134-5

Kimura, 1977, Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution, Nature, 267, 275, 10.1038/267275a0

Kimura, 1980, A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 16, 111, 10.1007/BF01731581

Kimura, 1983, The Neutral Theory of Molecular Evolution, 10.1017/CBO9780511623486

Kocken, 1993, Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum, Mol. Biochem. Parasitol., 61, 59, 10.1016/0166-6851(93)90158-T

Kocken, 1995, Minimal variation in the transmission-blocking vaccine candidate Pfs48/45 of the human malaria parasite Plasmodium falciparum, Mol. Biochem. Parasitol., 69, 115, 10.1016/0166-6851(94)00193-Q

Kondo, 1993, Evolution of hominoid mitochondrial DNA with special reference to the silent substitution rate over the genome, J. Mol. Evol., 36, 517, 10.1007/BF00556356

Kreitman, 1995, Molecular evidence for natural selection, Annu. Rev. Ecol. Syst., 26, 403, 10.1146/annurev.es.26.110195.002155

Krushkal, 1995, Substitution rates in hepatitis delta virus, J. Mol. Evol., 41, 721, 10.1007/BF00173151

Kumar, 1994, MEGA-Molecular Evolutionary Genetics Analysis Software for Microcomputers, Comput. Appl. Biosci., 10, 189

Lal, 1991, Circumsporozoite protein gene from Plasmodium reichenowi, a chimpanzee malaria parasite evolutionary related to the human malaria parasite Plasmodium falciparum, J. Biol. Chem., 266, 6686, 10.1016/S0021-9258(20)89552-0

Lal, 1990, Primary structure of the 25-kilodalton ookinete antigen from Plasmodium reichenowi, Mol. Biochem. Parasitol., 43, 143, 10.1016/0166-6851(90)90139-D

Li, 1993, Unbiased estimation of the rates of synonymous and nonsynonymous substitution, J. Mol. Evol., 36, 96, 10.1007/BF02407308

Li, 1991, Low nucleotide diversity in man, Genetics, 129, 513, 10.1093/genetics/129.2.513

Li, 1984, Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications, J. Mol. Evol., 21, 58, 10.1007/BF02100628

Liang, 1997, Conservation of structure and function of the erythrocyte-binding domain of Plasmodium falciparum EBA-175, Mol. Biochem. Parasitol., 84, 241, 10.1016/S0166-6851(96)02791-0

Lloyd, 1992, CODONS: a microcomputer program for codon usage analysis, J. Hered., 83, 239, 10.1093/oxfordjournals.jhered.a111205

Lockyer, 1987, Strain variation in the circumsporozoite protein gene of Plasmodium falciparum, Mol. Biochem. Parasitol., 22, 101, 10.1016/0166-6851(87)90073-9

Lockyer, 1989, Wild isolates of Plasmodium falciparum show extensive polymorphism in T cell epitopes of the circumsporozoite protein, Mol. Biochem. Parasitol., 37, 275, 10.1016/0166-6851(89)90159-X

Marsh, 1993, HLA Class-II nucleotide sequences, Immunogenetics, 37, 79, 10.1007/BF00216830

Marshall, 1991, A Plasmodium falciparum MSA-2 gene apparently generated by intragenic recombination between the two allelic families, Mol. Biochem. Parasitol., 45, 349, 10.1016/0166-6851(91)90104-E

Marshall, 1992, Two alleles within subfamilies of the merozoite surface protein antigen 2 (MSA-2) of Plasmodium falciparum, Mol. Biochem. Parasitol., 50, 181, 10.1016/0166-6851(92)90255-I

Maynard-Smith, 1994, Estimating selection by comparing synonymous and substitutional changes, J. Mol. Evol., 39, 123, 10.1007/BF00163800

McColl, 1994, Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites, Mol. Biochem. Parasitol., 68, 53, 10.1016/0166-6851(94)00149-9

McCutchan, 1984, Evolutionary relatedness of Plasmodium species as determined by the structure of DNA, Science, 225, 808, 10.1126/science.6382604

McCutchan, 1988, Antigenic diversity in Plasmodium falciparum, Prog. Allergy, 41, 173

McCutchan, 1992, Two types of sequence polymorphism in the circumsporozoite gene of Plasmodium falciparum, Mol. Biochem. Parasitol., 50, 37, 10.1016/0166-6851(92)90242-C

McDonald, 1991, Adaptive protein evolution at the Adh locus in Drosophila, Nature, 351, 652, 10.1038/351652a0

Miller, 1993, Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1), Mol. Biochem. Parasitol., 59, 1, 10.1016/0166-6851(93)90002-F

Mindell, 1996, Positive selection and rates of evolution in immunodeficiency viruses from humans and chimpanzees, Proc. Natl. Acad. Sci. USA, 93, 3284, 10.1073/pnas.93.8.3284

Moriyama, 1993, Codon usage bias and base composition of nuclear gene in Drosophila, Genetics, 134, 847, 10.1093/genetics/134.3.847

Musto, 1995, Compositional properties of nuclear genes from Plasmodium falciparum, Gene, 152, 127, 10.1016/0378-1119(94)00708-Z

Nei, 1987, Molecular Evolutionary Genetics, 10.7312/nei-92038

Nei, 1986, Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions, Mol. Biol. Evol., 3, 418

Oeuvray, 1994, Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes, Blood, 84, 1594, 10.1182/blood.V84.5.1594.1594

Ohta, 1992, The nearly neutral theory of molecular evolution, Annu. Rev. Ecol. Syst., 23, 263, 10.1146/annurev.es.23.110192.001403

Ohta, 1996, The neutralist-selectionist debate, Bioessays, 18, 673, 10.1002/bies.950180811

Oliveira, 1996, Genetic conservation of the Plasmodium falciparum apical membrane antigen-1 (AMA-1), Mol. Biochem. Parasitol., 76, 333, 10.1016/0166-6851(95)02548-0

Pan, 1995, A direct and rapid sequencing strategy for the Plasmodium falciparum antigen gene gp190/MSA1, Mol. Biochem. Parasitol., 73, 241, 10.1016/0166-6851(95)00094-H

Peterson, 1988, Variation in the precursor to the major merozoite surface antigens of Plasmodium falciparum, Mol. Biochem. Parasitol., 27, 291, 10.1016/0166-6851(88)90049-7

Peterson, 1989, Integral membrane protein located in the apical complex of Plasmodium falciparum, Mol. Cell. Biol., 9, 3151

Powell, 1997, Evolution of codon usage bias in Drosophila, Proc. Natl. Acad. Sci. USA, 94, 7784, 10.1073/pnas.94.15.7784

Rich, 1997, Plasmodium falciparum antigenic diversity: evidence of clonal population structure, Proc. Natl. Acad. Sci. USA, 94, 13040, 10.1073/pnas.94.24.13040

Ridley, 1990, Characterisation and sequence of a protective antigen from Plasmodium falciparum, Mol. Biochem. Parasitol., 41, 125, 10.1016/0166-6851(90)90103-S

Riley, 1994, Malaria, Parasitic Infections and the Immune System, 119, 10.1016/B978-0-08-092405-2.50008-4

Sawyer, 1989, Statistical test for detecting gene conversion, Mol. Biol. Evol., 6, 526

Sawyer, 1992, Population genetics of polymorphism and divergence, Genetics, 132, 1161, 10.1093/genetics/132.4.1161

Seibert, 1995, Natural selection on the gag, pol, and env genes of the human immunodeficiency virus 1 (HIV-1), Mol. Biol. Evol., 12, 803

Sharp, 1987, The rate of synonymous substitutions in eubacterial genes is inversely related to codon usage bias, Mol. Biol. Evol., 4, 222

Shi, 1992, Diversity in the immunodominant determinants of the circumsporozoite protein of Plasmodium falciparum parasites from malaria endemic regions of Papua New Guinea and Brazil, Am. J. Trop. Med. Hyg., 47, 844, 10.4269/ajtmh.1992.47.844

Shi, 1992, Single amino acid variation in the ookinete vaccine antigen from field isolates of Plasmodium falciparum, Mol. Biochem. Parasitol., 50, 179, 10.1016/0166-6851(92)90254-H

Shields, 1988, ‘Silent’ sited in Drosophila genes are not neutral: evidence of selection among synonymous codons, Mol. Biol. Evol., 5, 704

Sim, 1995, EBA-175—an erythrocyte-binding ligand of Plasmodium falciparum, Parasitol. Today, 6, 213

Simonsen, 1995, Properties of statistical tests of neutrality for DNA polymorphism data, Genetics, 141, 413, 10.1093/genetics/141.1.413

Smythe, 1990, Structural diversity in the 45-kilodalton merozoite surface antigen of Plasmodium falciparum, Mol. Biochem. Parasitol., 39, 227, 10.1016/0166-6851(90)90061-P

Sueoka, 1962, On the genetic basis of variation and heterogeneity on DNA base composition, Proc. Natl. Acad. Sci. USA, 48, 582, 10.1073/pnas.48.4.582

Sueoka, 1988, Directional mutation pressure and neutral molecular evolution, Proc. Natl. Acad. Sci. USA, 85, 2653, 10.1073/pnas.85.8.2653

Tajima, 1989, Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 123, 585, 10.1093/genetics/123.3.585

Tamura, 1992, Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C content biases, Mol. Biol. Evol., 9, 678

Tanabe, 1987, Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum, J. Mol. Biol., 195, 273, 10.1016/0022-2836(87)90649-8

Thomas, 1990, Sequence comparison of allelic forms of the Plasmodium falciparum merozoite surface antigen MSA-2, Mol. Biochem. Parasitol., 43, 211, 10.1016/0166-6851(90)90146-D

Tolle, 1995, Plasmodium falciparum: variations within the C-terminal region of merozoite surface antigen-1, Exp. Parasitol., 81, 47, 10.1006/expr.1995.1091

Vacquier, 1997, Positive Darwinian selection on two homologous fertilization proteins: what is the selection pressure driving their divergence?, J. Mol. Evol., 44, S15, 10.1007/PL00000049

Ware, 1993, Two alleles of the 175-kilodalton Plasmodium falciparum erythrocyte binding antigen, Mol. Biochem. Parasitol., 60, 105, 10.1016/0166-6851(93)90033-T

Weber, 1988, Merozoite surface protein sequence from the Camp strain of the human malaria parasite Plasmodium falciparum, Nucleic Acids Res., 16, 1206, 10.1093/nar/16.3.1206

Wolstenholme, 1985, Sequence evolution of Drosophila mitochondrial DNA, Genetics, 109, 725, 10.1093/genetics/109.4.725

World Health Organization, 1995, Tropical Disease Research, TDR Twelfth Program Report, 57

Wright, 1990, The ‘effective number of codons’ used in a gene, Gene, 87, 23, 10.1016/0378-1119(90)90491-9

Yang, 1995, Sequence variation in the non-repetitive regions of the liver stage-specific antigen-1 (LSA-1) of Plasmodium falciparum from field isolates, Mol. Biochem. Parasitol., 71, 291, 10.1016/0166-6851(95)00069-D

Zhu, 1991, Structure of Plasmodium falciparum liver stage antigen-1, Mol. Biochem. Parasitol., 48, 223, 10.1016/0166-6851(91)90117-O

Thông tin
Thông tin xuất bản

Genetics

Tập 149 Số 1

189-202

Thông tin tác giả