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Comparative Study
, 8, 108

Consistent and Contrasting Properties of Lineage-Specific Genes in the Apicomplexan Parasites Plasmodium and Theileria

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Comparative Study

Consistent and Contrasting Properties of Lineage-Specific Genes in the Apicomplexan Parasites Plasmodium and Theileria

Chih-Horng Kuo et al. BMC Evol Biol.

Abstract

Background: 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.

Results: 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.

Conclusion: 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.

Figures

Figure 1
Figure 1
The apicomplexan species tree. Maximum likelihood tree generated from the concatenated alignment of 83 single-copy genes (24,494 aligned amino acid sites). Two free-living ciliates, Paramecium tetraurelia and Tetrahymena thermophila, are included as the outgroup to root the tree. Labels above branches indicate the level of clade support inferred by 100 bootstrap replicates.
Figure 2
Figure 2
Phylogenetic distribution of orthologous gene clusters. The numbers after species name abbreviation (see Table 1) indicate the total number of annotated protein coding genes in the genome. The numbers above a branch and proceeded by a '+' sign indicate the number of orthologous gene clusters that are uniquely present in all daughter lineages; the numbers below a branch and proceeded by a '-' sign indicate the number of orthologous gene clusters that are uniquely absent. For example, on the internal branch that leads to the two Plasmodium species, 1,645 gene clusters contain sequences from both Pf and Pv but not any other species present on the tree. Similarly, there are 22 gene clusters that contain sequences from all species except Pf and Pv. Note that a gene cluster may contain more than one sequence from a species if paralogs are present in the genome. The levels refer to the degree of lineage specificity; genes in level 1 are shared by all species on the tree and genes in level 6 are species-specific.
Figure 3
Figure 3
Level of amino acid sequence divergence. The five categories on the X-axis refer to the level of lineage specificity defined in Figure 2. Level 6 genes are not included because they are species-specific and have no orthologous sequence for comparison. Error bars indicate standard errors.
Figure 4
Figure 4
(G + C) content at the third codon position. The level of lineage specificity for each calculation is as defined in Figure 2. Error bars indicate standard errors.
Figure 5
Figure 5
Chromosomal location of genes in Plasmodium falciparum. Chromosomal location of genes on P. falciparum chromosome 10. See Additional file 4 for views of all 14 chromosomes in this species. The level of lineage specificity is as defined in Figure 2. A. View of entire chromosome 10 (MAL10). B. Close-up view of the first 200 kb of chromosome 10.
Figure 6
Figure 6
Chromosomal location of genes in Theileria annulata. Chromosomal location of genes on T. annulata chromosome 2. See Additional file 5 for views of all four chromosomes in this species. The level of lineage specificity is as defined in Figure 2. A. View of entire chromosome 2. B. Close-up view of the first 200 kb of chromosome 2.
Figure 7
Figure 7
Average and minimal distance of mapped genes to chromosome end. The level of lineage specificity is as defined in Figure 2. A. Average distance to chromosome end in Plasmodium falciparum. B. Minimum distance to chromosome end in P. falciparum. C. Average distance to chromosome end in Theileria annulata. B. Minimum distance to chromosome end in T. annulata.
Figure 8
Figure 8
Amino acid sequence divergence and chromosomal location. Plot of amino acid sequence divergence as a function of the distance to the nearest chromosome end. A. Plasmodium falciparum. B. Theileria annulata. The black lines in both panels (i.e., Pf1-5 in panel A and Ta1-5 in panel B) refer to the combined results from genes with five different levels of lineage specificity and are included as the background reference. Error bars indicate standard errors.

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