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      Two Hybridization Events Define the Population Structure of Trypanosoma cruzi

      , , ,
      Genetics
      Genetics Society of America

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          Abstract

          Genetic variation in Trypanosoma cruzi is likely a key determinant in transmission and pathogenesis of Chagas disease. We have examined nine loci as markers for the extant T. cruzi strains. Four distinct alleles were found for each locus, corresponding to the sequence classes present in the homozygous discrete typing units (DTUs) I, IIa, IIb, and IIc. The alleles in DTUs IIa and IIc showed a spectrum of polymorphism ranging from DTU I-like to DTU IIb-like, in addition to DTU-specific sequence variation. DTUs IId and IIe were indistinguishable, showing DTU homozygosity at one locus and heterozygosity with DTU IIb and IIc allelic sequences at eight loci. Recombination between the DTU IIb and IIc alleles is evidenced from mosaic polymorphisms. These data imply that two discrete hybridization events resulted in the formation of the current DTUs. We propose a model in which a fusion between ancestral DTU I and IIb strains gave rise to a heterozygous hybrid that homogenized its genome to become the homozygous progenitor of DTUs IIa and IIc. The second hybridization between DTU IIb and IIc strains that generated DTUs IId and IIe resulted in extensive heterozygosity with subsequent recombination of parental genotypes.

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          Most cited references57

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          Mechanism of genetic exchange in American trypanosomes.

          The kinetoplastid Protozoa are responsible for devastating diseases. In the Americas, Trypanosoma cruzi is the agent of Chagas' disease--a widespread disease transmissible from animals to humans (zoonosis)--which is transmitted by exposure to infected faeces of blood-sucking triatomine bugs. The presence of genetic exchange in T. cruzi and in Leishmania is much debated. Here, by producing hybrid clones, we show that T. cruzi has an extant capacity for genetic exchange. The mechanism is unusual and distinct from that proposed for the African trypanosome, Trypanosoma brucei. Two biological clones of T. cruzi were transfected to carry different drug-resistance markers, and were passaged together through the entire life cycle. Six double-drug-resistant progeny clones, recovered from the mammalian stage of the life cycle, show fusion of parental genotypes, loss of alleles, homologous recombination, and uniparental inheritance of kinetoplast maxicircle DNA. There are strong genetic parallels between these experimental hybrids and the genotypes among natural isolates of T. cruzi. In this instance, aneuploidy through nuclear hybridization results in recombination across far greater genetic distances than mendelian genetic exchange. This mechanism also parallels genome duplication.
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            DNA markers define two major phylogenetic lineages of Trypanosoma cruzi.

            R. Souto (1996)
            Parasitic protozoa within the taxon Trypanosoma cruzi are considered to be derived from multiple clonal lineages, and show broad genetic diversity as a result of propagation with little or no genetic exchange. We have analyzed a wide sample of T. cruzi isolates from vertebrate and invertebrate hosts by PCR amplification of a ribosomal RNA gene sequence, a mini-exon gene sequence and random amplified polymorphic DNA (RAPD). Amplification of the distinct rDNA and mini-exon gene sequences indicated a dimorphism within both of the tandemly-repeated genes: 125 or 110 bp products for rDNA and 300 or 350 bp products for the mini-exon. Within individual isolates, one of three associations was observed: the 125 bp rDNA product with the 300 bp mini-exon product (defined as group 1), the 110 bp rDNA product with the 350 bp mini-exon product (defined as group 2) and the presence of both rDNA amplification products with the mini-exon group 1 product (group 1/2). The RAPD analysis showed variability between individual isolates, however, tree analysis clearly indicated the presence of two major branches. Interestingly, the rDNA/mini-exon group 2 isolates correlated precisely with one branch of the RAPD-derived tree; group 1 and group 1/2 isolates correlated with the other branch. Our studies show a clear division of T. cruzi into two major lineages presenting a high phylogenetic divergence. Hypotheses are discussed to explain the origin of the two lineages as well as isolates that are hybrid for group 1 and 2 rDNA markers.
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              Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi.

              Simple phylogenetic tests were applied to a large data set of nucleotide sequences from two nuclear genes and a region of the mitochondrial genome of Trypanosoma cruzi, the agent of Chagas' disease. Incongruent gene genealogies manifest genetic exchange among distantly related lineages of T. cruzi. Two widely distributed isoenzyme types of T. cruzi are hybrids, their genetic composition being the likely result of genetic exchange between two distantly related lineages. The data show that the reference strain for the T. cruzi genome project (CL Brener) is a hybrid. Well-supported gene genealogies show that mitochondrial and nuclear gene sequences from T. cruzi cluster, respectively, in three or four distinct clades that do not fully correspond to the two previously defined major lineages of T. cruzi. There is clear genetic differentiation among the major groups of sequences, but genetic diversity within each major group is low. We estimate that the major extant lineages of T. cruzi have diverged during the Miocene or early Pliocene (3-16 million years ago).
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                Author and article information

                Journal
                Genetics
                Genetics
                Genetics Society of America
                0016-6731
                1943-2631
                October 25 2005
                October 2005
                October 2005
                July 05 2005
                : 171
                : 2
                : 527-543
                Article
                10.1534/genetics.104.038745
                1456769
                15998728
                1b3010a3-d247-4b07-8dbb-c206be3020c8
                © 2005
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