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Evolution of long centromeres in fire ants

BACKGROUND: Centromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species. Centromere drive predicts rapid turnover because some centromeric sequences may compete better than others during female meiosis. In addition to sequence co...

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Autores principales: Huang, Yu-Ching, Lee, Chih-Chi, Kao, Chia-Yi, Chang, Ni-Chen, Lin, Chung-Chi, Shoemaker, DeWayne, Wang, John
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5024525/
https://www.ncbi.nlm.nih.gov/pubmed/27628313
http://dx.doi.org/10.1186/s12862-016-0760-7
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author Huang, Yu-Ching
Lee, Chih-Chi
Kao, Chia-Yi
Chang, Ni-Chen
Lin, Chung-Chi
Shoemaker, DeWayne
Wang, John
author_facet Huang, Yu-Ching
Lee, Chih-Chi
Kao, Chia-Yi
Chang, Ni-Chen
Lin, Chung-Chi
Shoemaker, DeWayne
Wang, John
author_sort Huang, Yu-Ching
collection PubMed
description BACKGROUND: Centromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species. Centromere drive predicts rapid turnover because some centromeric sequences may compete better than others during female meiosis. In addition to sequence composition, longer centromeres may have a transmission advantage. RESULTS: We report the first observations of extremely long centromeres, covering on average 34 % of the chromosomes, in the red imported fire ant Solenopsis invicta. By comparison, cytological examination of Solenopsis geminata revealed typical small centromeric constrictions. Bioinformatics and molecular analyses identified CenSol, the major centromeric satellite DNA repeat. We found that CenSol sequences are very similar between the two species but the CenSol copy number in S. invicta is much greater than that in S. geminata. In addition, centromere expansion in S. invicta is not correlated with the duplication of CenH3. Comparative analyses revealed that several closely related fire ant species also possess long centromeres. CONCLUSIONS: Our results are consistent with a model of simple runaway centromere expansion due to centromere drive. We suggest expanded centromeres may be more prevalent in hymenopteran insects, which use haplodiploid sex determination, than previously considered. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0760-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-50245252016-09-20 Evolution of long centromeres in fire ants Huang, Yu-Ching Lee, Chih-Chi Kao, Chia-Yi Chang, Ni-Chen Lin, Chung-Chi Shoemaker, DeWayne Wang, John BMC Evol Biol Research Article BACKGROUND: Centromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species. Centromere drive predicts rapid turnover because some centromeric sequences may compete better than others during female meiosis. In addition to sequence composition, longer centromeres may have a transmission advantage. RESULTS: We report the first observations of extremely long centromeres, covering on average 34 % of the chromosomes, in the red imported fire ant Solenopsis invicta. By comparison, cytological examination of Solenopsis geminata revealed typical small centromeric constrictions. Bioinformatics and molecular analyses identified CenSol, the major centromeric satellite DNA repeat. We found that CenSol sequences are very similar between the two species but the CenSol copy number in S. invicta is much greater than that in S. geminata. In addition, centromere expansion in S. invicta is not correlated with the duplication of CenH3. Comparative analyses revealed that several closely related fire ant species also possess long centromeres. CONCLUSIONS: Our results are consistent with a model of simple runaway centromere expansion due to centromere drive. We suggest expanded centromeres may be more prevalent in hymenopteran insects, which use haplodiploid sex determination, than previously considered. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0760-7) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-15 /pmc/articles/PMC5024525/ /pubmed/27628313 http://dx.doi.org/10.1186/s12862-016-0760-7 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Huang, Yu-Ching
Lee, Chih-Chi
Kao, Chia-Yi
Chang, Ni-Chen
Lin, Chung-Chi
Shoemaker, DeWayne
Wang, John
Evolution of long centromeres in fire ants
title Evolution of long centromeres in fire ants
title_full Evolution of long centromeres in fire ants
title_fullStr Evolution of long centromeres in fire ants
title_full_unstemmed Evolution of long centromeres in fire ants
title_short Evolution of long centromeres in fire ants
title_sort evolution of long centromeres in fire ants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5024525/
https://www.ncbi.nlm.nih.gov/pubmed/27628313
http://dx.doi.org/10.1186/s12862-016-0760-7
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