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NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii

BACKGROUND: Toxoplasma gondii is a widespread protozoan parasite of animals that causes zoonotic disease in humans. Three clonal variants predominate in North America and Europe, while South American strains are genetically diverse, and undergo more frequent recombination. All three northern clonal...

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Autores principales: Khan, Asis, Shaik, Jahangheer S, Behnke, Michael, Wang, Qiuling, Dubey, Jitender P, Lorenzi, Hernan A, Ajioka, James W, Rosenthal, Benjamin M, Sibley, L David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4326188/
https://www.ncbi.nlm.nih.gov/pubmed/25532601
http://dx.doi.org/10.1186/1471-2164-15-1168
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author Khan, Asis
Shaik, Jahangheer S
Behnke, Michael
Wang, Qiuling
Dubey, Jitender P
Lorenzi, Hernan A
Ajioka, James W
Rosenthal, Benjamin M
Sibley, L David
author_facet Khan, Asis
Shaik, Jahangheer S
Behnke, Michael
Wang, Qiuling
Dubey, Jitender P
Lorenzi, Hernan A
Ajioka, James W
Rosenthal, Benjamin M
Sibley, L David
author_sort Khan, Asis
collection PubMed
description BACKGROUND: Toxoplasma gondii is a widespread protozoan parasite of animals that causes zoonotic disease in humans. Three clonal variants predominate in North America and Europe, while South American strains are genetically diverse, and undergo more frequent recombination. All three northern clonal variants share a monomorphic version of chromosome Ia (ChrIa), which is also found in unrelated, but successful southern lineages. Although this pattern could reflect a selective advantage, it might also arise from non-Mendelian segregation during meiosis. To understand the inheritance of ChrIa, we performed a genetic cross between the northern clonal type 2 ME49 strain and a divergent southern type 10 strain called VAND, which harbors a divergent ChrIa. RESULTS: NextGen sequencing of haploid F1 progeny was used to generate a genetic map revealing a low level of conventional recombination, with an unexpectedly high frequency of short, double crossovers. Notably, both the monomorphic and divergent versions of ChrIa were isolated with equal frequency. As well, ChrIa showed no evidence of being a sex chromosome, of harboring an inversion, or distorting patterns of segregation. Although VAND was unable to self fertilize in the cat, it underwent successful out-crossing with ME49 and hybrid survival was strongly associated with inheritance of ChrIII from ME49 and ChrIb from VAND. CONCLUSIONS: Our findings suggest that the successful spread of the monomorphic ChrIa in the wild has not been driven by meiotic drive or related processes, but rather is due to a fitness advantage. As well, the high frequency of short double crossovers is expected to greatly increase genetic diversity among progeny from genetic crosses, thereby providing an unexpected and likely important source of diversity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1168) contains supplementary material, which is available to authorized users.
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spelling pubmed-43261882015-02-13 NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii Khan, Asis Shaik, Jahangheer S Behnke, Michael Wang, Qiuling Dubey, Jitender P Lorenzi, Hernan A Ajioka, James W Rosenthal, Benjamin M Sibley, L David BMC Genomics Research Article BACKGROUND: Toxoplasma gondii is a widespread protozoan parasite of animals that causes zoonotic disease in humans. Three clonal variants predominate in North America and Europe, while South American strains are genetically diverse, and undergo more frequent recombination. All three northern clonal variants share a monomorphic version of chromosome Ia (ChrIa), which is also found in unrelated, but successful southern lineages. Although this pattern could reflect a selective advantage, it might also arise from non-Mendelian segregation during meiosis. To understand the inheritance of ChrIa, we performed a genetic cross between the northern clonal type 2 ME49 strain and a divergent southern type 10 strain called VAND, which harbors a divergent ChrIa. RESULTS: NextGen sequencing of haploid F1 progeny was used to generate a genetic map revealing a low level of conventional recombination, with an unexpectedly high frequency of short, double crossovers. Notably, both the monomorphic and divergent versions of ChrIa were isolated with equal frequency. As well, ChrIa showed no evidence of being a sex chromosome, of harboring an inversion, or distorting patterns of segregation. Although VAND was unable to self fertilize in the cat, it underwent successful out-crossing with ME49 and hybrid survival was strongly associated with inheritance of ChrIII from ME49 and ChrIb from VAND. CONCLUSIONS: Our findings suggest that the successful spread of the monomorphic ChrIa in the wild has not been driven by meiotic drive or related processes, but rather is due to a fitness advantage. As well, the high frequency of short double crossovers is expected to greatly increase genetic diversity among progeny from genetic crosses, thereby providing an unexpected and likely important source of diversity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1168) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-23 /pmc/articles/PMC4326188/ /pubmed/25532601 http://dx.doi.org/10.1186/1471-2164-15-1168 Text en © Khan et al.; licensee BioMed Central. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Khan, Asis
Shaik, Jahangheer S
Behnke, Michael
Wang, Qiuling
Dubey, Jitender P
Lorenzi, Hernan A
Ajioka, James W
Rosenthal, Benjamin M
Sibley, L David
NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title_full NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title_fullStr NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title_full_unstemmed NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title_short NextGen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in Toxoplasma gondii
title_sort nextgen sequencing reveals short double crossovers contribute disproportionately to genetic diversity in toxoplasma gondii
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4326188/
https://www.ncbi.nlm.nih.gov/pubmed/25532601
http://dx.doi.org/10.1186/1471-2164-15-1168
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