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PMID: 18405380 Published · epublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Consistent and contrasting properties of lineage-specific genes in the apicomplexan parasites Plasmodium and Theileria.

BMC evolutionary biology ·Vol. 8 ·2008-04-11 ·Pages 108

Kuo CH, Kissinger JC

Abstract

Lineage-specific genes, the genes that are restricted to a limited subset of related organisms, may be important in adaptation. In parasitic organisms, lineage-specific gene products are possible targets for vaccine development or therapeutics when these genes are absent from the host genome. In this study, we utilized comparative approaches based on a phylogenetic framework to characterize lineage-specific genes in the parasitic protozoan phylum Apicomplexa. Genes from species in two major apicomplexan genera, Plasmodium and Theileria, were categorized into six levels of lineage specificity based on a nine-species phylogeny. In both genera, lineage-specific genes tend to have a higher level of sequence divergence among sister species. In addition, species-specific genes possess a strong codon usage bias compared to other genes in the genome. We found that a large number of genus- or species-specific genes are putative surface antigens that may be involved in host-parasite interactions. Interestingly, the two parasite lineages exhibit several notable differences. In Plasmodium, the (G + C) content at the third codon position increases with lineage specificity while Theileria shows the opposite trend. Surface antigens in Plasmodium are species-specific and mainly located in sub-telomeric regions. In contrast, surface antigens in Theileria are conserved at the genus level and distributed across the entire lengths of chromosomes. Our results provide further support for the model that gene duplication followed by rapid divergence is a major mechanism for generating lineage-specific genes. The result that many lineage-specific genes are putative surface antigens supports the hypothesis that lineage-specific genes could be important in parasite adaptation. The contrasting properties between the lineage-specific genes in two major apicomplexan genera indicate that the mechanisms of generating lineage-specific genes and the subsequent evolutionary fates can differ between related parasite lineages. Future studies that focus on improving functional annotation of parasite genomes and collection of genetic variation data at within- and between-species levels will be important in facilitating our understanding of parasite adaptation and natural selection.

MeSH Terms
Amino Acid Sequence Animals Base Composition Base Sequence Chromosome Mapping Codon Evolution, Molecular Genes, Protozoan Genetic Speciation Genetic Variation Multigene Family Phylogeny Plasmodium/classification,genetics Plasmodium falciparum/genetics Theileria/classification,genetics Theileria annulata/genetics
Chemicals
Codon
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kuo Chih-Horng
Department of Genetics, University of Georgia, Athens, GA 30602, USA. [email protected]
Kissinger Jessica C
References (78)
78 references, click to expand
  1. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.
    Mol Biol Evol. 2000 Apr;17(4):540-52 PMID: 10742046
  2. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5793-7 PMID: 7597031
  3. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia.
    Nature. 2006 Nov 9;444(7116):171-8 PMID: 17086204
  4. Evolution of hydra, a recently evolved testis-expressed gene with nine alternative first exons in Drosophila melanogaster.
    PLoS Genet. 2007 Jul;3(7):e107 PMID: 17616977
  5. Phylogenomics of eukaryotes: impact of missing data on large alignments.
    Mol Biol Evol. 2004 Sep;21(9):1740-52 PMID: 15175415
  6. The genome of Cryptosporidium hominis.
    Nature. 2004 Oct 28;431(7012):1107-12 PMID: 15510150
  7. Complete genome sequence of the apicomplexan, Cryptosporidium parvum.
    Science. 2004 Apr 16;304(5669):441-5 PMID: 15044751
  8. Large-scale intron conservation and order-of-magnitude variation in intron loss/gain rates in apicomplexan evolution.
    Genome Res. 2006 Oct;16(10):1270-5 PMID: 16963708
  9. The Pfam protein families database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41 PMID: 14681378
  10. Plasmodium falciparum variant surface antigen expression patterns during malaria.
    PLoS Pathog. 2005 Nov;1(3):e26 PMID: 16304608
  11. Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli.
    Genome Res. 2004 Jun;14(6):1036-42 PMID: 15173110
  12. ParameciumDB: a community resource that integrates the Paramecium tetraurelia genome sequence with genetic data.
    Nucleic Acids Res. 2007 Jan;35(Database issue):D439-44 PMID: 17142227
  13. Inverse relationship between evolutionary rate and age of mammalian genes.
    Mol Biol Evol. 2005 Mar;22(3):598-606 PMID: 15537804
  14. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.
    Nucleic Acids Res. 1987 Feb 11;15(3):1281-95 PMID: 3547335
  15. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum.
    Nature. 2000 Oct 26;407(6807):1018-22 PMID: 11069183
  16. Discovery of gene function by expression profiling of the malaria parasite life cycle.
    Science. 2003 Sep 12;301(5639):1503-8 PMID: 12893887
  17. Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression.
    Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9935-9 PMID: 16777968
  18. Telomere structure and function in trypanosomes: a proposal.
    Nat Rev Microbiol. 2007 Jan;5(1):70-5 PMID: 17160000
  19. Evolutionary origins of genomic repertoires in bacteria.
    PLoS Biol. 2005 May;3(5):e130 PMID: 15799709
  20. The evolutionary analysis of "orphans" from the Drosophila genome identifies rapidly diverging and incorrectly annotated genes.
    Genetics. 2001 Oct;159(2):589-98 PMID: 11606536
  21. Horizontal gene transfer, genome innovation and evolution.
    Nat Rev Microbiol. 2005 Sep;3(9):679-87 PMID: 16138096
  22. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes.
    Science. 2005 Jul 1;309(5731):134-7 PMID: 15994558
  23. Codon usages in different gene classes of the Escherichia coli genome.
    Mol Microbiol. 1998 Sep;29(6):1341-55 PMID: 9781873
  24. Prokaryotic RNA preparation methods useful for high density array analysis: comparison of two approaches.
    Nucleic Acids Res. 2001 Nov 15;29(22):E112 PMID: 11713332
  25. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences.
    J Parasitol. 2002 Oct;88(5):972-8 PMID: 12435139
  26. Comparative genomics of the eukaryotes.
    Science. 2000 Mar 24;287(5461):2204-15 PMID: 10731134
  27. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes.
    Science. 2007 Sep 21;317(5845):1753-6 PMID: 17761848
  28. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae.
    Nature. 2004 Apr 8;428(6983):617-24 PMID: 15004568
  29. PAML 4: phylogenetic analysis by maximum likelihood.
    Mol Biol Evol. 2007 Aug;24(8):1586-91 PMID: 17483113
  30. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
    Bioinformatics. 2002 Mar;18(3):502-4 PMID: 11934758
  31. Finding families for genomic ORFans.
    Bioinformatics. 1999 Sep;15(9):759-62 PMID: 10498776
  32. A first glimpse into the pattern and scale of gene transfer in Apicomplexa.
    Int J Parasitol. 2004 Mar 9;34(3):265-74 PMID: 15003488
  33. CryptoDB: a Cryptosporidium bioinformatics resource update.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D419-22 PMID: 16381902
  34. Nuclear architecture underlying gene expression in Trypanosoma brucei.
    Trends Microbiol. 2007 Jun;15(6):263-70 PMID: 17481901
  35. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12 PMID: 16845082
  36. On homology searches by protein Blast and the characterization of the age of genes.
    BMC Evol Biol. 2007 Apr 04;7:53 PMID: 17408474
  37. PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data.
    Nucleic Acids Res. 2003 Jan 1;31(1):212-5 PMID: 12519984
  38. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?
    Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15386-91 PMID: 15494441
  39. Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family.
    Mol Microbiol. 2003 Dec;50(5):1527-38 PMID: 14651636
  40. Origin and evolution of new exons in rodents.
    Genome Res. 2005 Sep;15(9):1258-64 PMID: 16109974
  41. Genome sequence of the human malaria parasite Plasmodium falciparum.
    Nature. 2002 Oct 3;419(6906):498-511 PMID: 12368864
  42. The "inverse relationship between evolutionary rate and age of mammalian genes" is an artifact of increased genetic distance with rate of evolution and time of divergence.
    Mol Biol Evol. 2006 Jan;23(1):1-3 PMID: 16151190
  43. Common themes in the genome strategies of pathogens.
    Curr Opin Genet Dev. 2005 Dec;15(6):584-8 PMID: 16188434
  44. Orphans as taxonomically restricted and ecologically important genes.
    Microbiology (Reading). 2005 Aug;151(Pt 8):2499-2501 PMID: 16079329
  45. ToxoDB: an integrated Toxoplasma gondii database resource.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D553-6 PMID: 18003657
  46. OrthoMCL: identification of ortholog groups for eukaryotic genomes.
    Genome Res. 2003 Sep;13(9):2178-89 PMID: 12952885
  47. Genome evolution and the evolution of exon-shuffling--a review.
    Gene. 1999 Sep 30;238(1):103-14 PMID: 10570989
  48. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
    Syst Biol. 2003 Oct;52(5):696-704 PMID: 14530136
  49. A Plasmodium whole-genome synteny map: indels and synteny breakpoints as foci for species-specific genes.
    PLoS Pathog. 2005 Dec;1(4):e44 PMID: 16389297
  50. The gain and loss of genes during 600 million years of vertebrate evolution.
    Genome Biol. 2006;7(5):R43 PMID: 16723033
  51. Comparative DNA analysis across diverse genomes.
    Annu Rev Genet. 1998;32:185-225 PMID: 9928479
  52. Exon shuffling by L1 retrotransposition.
    Science. 1999 Mar 5;283(5407):1530-4 PMID: 10066175
  53. Distance from the chromosome end determines the efficiency of double strand break repair in subtelomeres of haploid yeast.
    J Mol Biol. 2003 May 9;328(4):847-62 PMID: 12729759
  54. Nucleotide composition bias affects amino acid content in proteins coded by animal mitochondria.
    J Mol Evol. 1997 Mar;44(3):282-8 PMID: 9060394
  55. Accelerated evolutionary rate may be responsible for the emergence of lineage-specific genes in ascomycota.
    J Mol Evol. 2006 Jul;63(1):1-11 PMID: 16755356
  56. Plasmodium telomeres: a pathogen's perspective.
    Curr Opin Microbiol. 2001 Aug;4(4):409-14 PMID: 11495803
  57. Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication.
    Nature. 2005 Sep 1;437(7055):94-100 PMID: 16136133
  58. Predicted highly expressed genes of diverse prokaryotic genomes.
    J Bacteriol. 2000 Sep;182(18):5238-50 PMID: 10960111
  59. An evolutionary analysis of orphan genes in Drosophila.
    Genome Res. 2003 Oct;13(10):2213-9 PMID: 14525923
  60. Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3497-502 PMID: 8622965
  61. The generic genome browser: a building block for a model organism system database.
    Genome Res. 2002 Oct;12(10):1599-610 PMID: 12368253
  62. Population genomics of the immune evasion (var) genes of Plasmodium falciparum.
    PLoS Pathog. 2007 Mar;3(3):e34 PMID: 17367208
  63. A systematic map of genetic variation in Plasmodium falciparum.
    PLoS Pathog. 2006 Jun;2(6):e57 PMID: 16789840
  64. Regulation of vsg expression site transcription and switching in Trypanosoma brucei.
    Mol Biochem Parasitol. 1998 Mar 1;91(1):77-91 PMID: 9574927
  65. Natural variation in a subtelomeric region of Arabidopsis: implications for the genomic dynamics of a chromosome end.
    Genetics. 2006 May;173(1):401-17 PMID: 16547105
  66. Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of apicomplexa.
    Mol Biol Evol. 1997 Apr;14(4):428-41 PMID: 9100373
  67. Toxoplasmosis.
    Lancet. 2004 Jun 12;363(9425):1965-76 PMID: 15194258
  68. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum.
    Cell. 2005 Apr 8;121(1):13-24 PMID: 15820675
  69. GeneDB: a resource for prokaryotic and eukaryotic organisms.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D339-43 PMID: 14681429
  70. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  71. The K(A)/K(S) ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study.
    Genome Res. 2002 Jan;12(1):198-202 PMID: 11779845
  72. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote.
    PLoS Biol. 2006 Sep;4(9):e286 PMID: 16933976
  73. Distinguishing the ORFs from the ELFs: short bacterial genes and the annotation of genomes.
    Trends Genet. 2002 Jul;18(7):335-7 PMID: 12127765
  74. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva.
    Science. 2005 Jul 1;309(5731):131-3 PMID: 15994557
  75. Lateral gene transfer and the nature of bacterial innovation.
    Nature. 2000 May 18;405(6784):299-304 PMID: 10830951
  76. Gene transfer in the evolution of parasite nucleotide biosynthesis.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3154-9 PMID: 14973196
  77. The rapid generation of mutation data matrices from protein sequences.
    Comput Appl Biosci. 1992 Jun;8(3):275-82 PMID: 1633570
  78. Why are parasite contingency genes often associated with telomeres?
    Int J Parasitol. 2003 Jan;33(1):29-45 PMID: 12547344
Article Info
Journal
BMC evolutionary biology
Abbr.
BMC Evol Biol
ISSN
1471-2148
Published
2008-04-11
Epub
2008-00-11
Pages
108
Language
English
Region
England
NLM ID
100966975
PMCID
PMC2330040
Subset
IM
Grants
NIAID NIH HHS · R01 AI068908 · United States
NIAID NIH HHS · R01 AI068908-01A2 · United States
NIGMS NIH HHS · GM07103 · United States
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