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Comparative Study
. 2006 Sep;16(9):1119-25.
doi: 10.1101/gr.5318106. Epub 2006 Aug 10.

Common inheritance of chromosome Ia associated with clonal expansion of Toxoplasma gondii

Asis Khan  1 , Ulrike Böhme, Krystyna A Kelly, Ellen Adlem, Karen Brooks, Mark Simmonds, Karen Mungall, Michael A Quail, Claire Arrowsmith, Tracey Chillingworth, Carol Churcher, David Harris, Matthew Collins, Nigel Fosker, Audrey Fraser, Zahra Hance, Kay Jagels, Sharon Moule, Lee Murphy, Susan O'Neil, Marie-Adele Rajandream, David Saunders, Kathy Seeger, Sally Whitehead, Thomas Mayr, Xuenan Xuan, Junichi Watanabe, Yutaka Suzuki, Hiroyuki Wakaguri, Sumio Sugano, Chihiro Sugimoto, Ian Paulsen, Aaron J Mackey, David S Roos, Neil Hall, Matthew Berriman, Bart Barrell, L David Sibley, James W Ajioka
Affiliations
Comparative Study

Common inheritance of chromosome Ia associated with clonal expansion of Toxoplasma gondii

Asis Khan et al. Genome Res. 2006 Sep.

Abstract

Toxoplasma gondii is a globally distributed protozoan parasite that can infect virtually all warm-blooded animals and humans. Despite the existence of a sexual phase in the life cycle, T. gondii has an unusual population structure dominated by three clonal lineages that predominate in North America and Europe, (Types I, II, and III). These lineages were founded by common ancestors approximately10,000 yr ago. The recent origin and widespread distribution of the clonal lineages is attributed to the circumvention of the sexual cycle by a new mode of transmission-asexual transmission between intermediate hosts. Asexual transmission appears to be multigenic and although the specific genes mediating this trait are unknown, it is predicted that all members of the clonal lineages should share the same alleles. Genetic mapping studies suggested that chromosome Ia was unusually monomorphic compared with the rest of the genome. To investigate this further, we sequenced chromosome Ia and chromosome Ib in the Type I strain, RH, and the Type II strain, ME49. Comparative genome analyses of the two chromosomal sequences revealed that the same copy of chromosome Ia was inherited in each lineage, whereas chromosome Ib maintained the same high frequency of between-strain polymorphism as the rest of the genome. Sampling of chromosome Ia sequence in seven additional representative strains from the three clonal lineages supports a monomorphic inheritance, which is unique within the genome. Taken together, our observations implicate a specific combination of alleles on chromosome Ia in the recent origin and widespread success of the clonal lineages of T. gondii.

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Figures

Figure 1.
Figure 1.
Single Nucleotide Polymorphisms (SNPs) on chromosome Ia vs. chromosome Ib for the RH vs. ME49 comparison. Distribution of SNPs (counts per 2000 bp). chrIa has 332 SNPs, chrIb has 12,925 SNPs.
Figure 2.
Figure 2.
Composition of chrIa for clonal (I, II, III) strains based on sequence analysis of 26 regions. Yellow represents areas not sequenced in the alternative strains, white represents sequenced areas that are identical to RH and ME49, and red represents regions containing a single SNP. Twelve regions are represented in all nine strains. Only two SNPs are seen in these 12 regions, which represents a total of 86,814 bp of sequence across the nine strains.
Figure 3.
Figure 3.
Progeny from genetic crosses between the Type I and Type III lineage were analyzed using six polymorphic markers on each of chrIa and chrIb. The resulting allele patterns are shown for each of 31 progeny at each locus (solid boxes, Type III lineage; open boxes, Type I lineage). Progeny where recombination has occurred are indicated at the bottom by an asterisk. The maps at the top represent the linear genetic maps for each chromosome with the markers shown on the right and the genetic distances shown on the left in centiMorgans.
Figure 4.
Figure 4.
Model of the evolutionary histories of chrIa and chrIb. (A) Original A&E cross. (A) blue; (E) pink; (shorter bar) chrIa; (longer bar) chrIb. (B) Recombinant progeny from a restricted gene pool. A special chrIa (black outline), generated by recombination, carries allele(s) that allow or enhance transmission between intermediate hosts, permitting asexual propagation and suppressing recombination events that might break up the special combination of alleles. (C) Asexual growth expands the lineage in the population. Infrequent sexual events with highly recombinant relatives from the original cross allow parasites with the special chromosome Ia to acquire highly recombinant chromosomes including chromosome Ib. These new recombinant parasites can now expand in the population through asexual growth. (D) Natural selection for asexual growth maintains the special chrIa intact and three different clonal lineages (i.e., Types I, II, and III) expand and become predominant in the population.
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