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Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor

BACKGROUND: The availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative m...

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Autores principales: Romanov, Michael N, Farré, Marta, Lithgow, Pamela E, Fowler, Katie E, Skinner, Benjamin M, O’Connor, Rebecca, Fonseka, Gothami, Backström, Niclas, Matsuda, Yoichi, Nishida, Chizuko, Houde, Peter, Jarvis, Erich D, Ellegren, Hans, Burt, David W, Larkin, Denis M, Griffin, Darren K
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4362836/
https://www.ncbi.nlm.nih.gov/pubmed/25496766
http://dx.doi.org/10.1186/1471-2164-15-1060
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author Romanov, Michael N
Farré, Marta
Lithgow, Pamela E
Fowler, Katie E
Skinner, Benjamin M
O’Connor, Rebecca
Fonseka, Gothami
Backström, Niclas
Matsuda, Yoichi
Nishida, Chizuko
Houde, Peter
Jarvis, Erich D
Ellegren, Hans
Burt, David W
Larkin, Denis M
Griffin, Darren K
author_facet Romanov, Michael N
Farré, Marta
Lithgow, Pamela E
Fowler, Katie E
Skinner, Benjamin M
O’Connor, Rebecca
Fonseka, Gothami
Backström, Niclas
Matsuda, Yoichi
Nishida, Chizuko
Houde, Peter
Jarvis, Erich D
Ellegren, Hans
Burt, David W
Larkin, Denis M
Griffin, Darren K
author_sort Romanov, Michael N
collection PubMed
description BACKGROUND: The availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative molecular cytogenetics of only the largest chromosomes. Here, novel whole genome sequence information from 21 avian genome sequences (most newly assembled) made available on an interactive browser (Evolution Highway) was analyzed. RESULTS: Focusing on the six best-assembled genomes allowed us to assemble a putative karyotype of the dinosaur ancestor for each chromosome. Reconstructing evolutionary events that led to each species’ genome organization, we determined that the fastest rate of change occurred in the zebra finch and budgerigar, consistent with rapid speciation events in the Passeriformes and Psittaciformes. Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace. Analyzing chicken and zebra finch, we found little evidence to support the hypothesis of an association of evolutionary breakpoint regions with recombination hotspots but some evidence to support the hypothesis that microchromosomes largely represent conserved blocks of synteny in the majority of the 21 species analyzed. All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count. Ostrich, however, appeared to retain an overall karyotype structure of 2n = 80 despite undergoing a large number (26) of hitherto un-described interchromosomal changes. CONCLUSIONS: Results suggest that mechanisms exist to preserve a static overall avian karyotype/genomic structure, including the microchromosomes, with widespread interchromosomal change occurring rarely (e.g., in ostrich and budgerigar lineages). Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1060) contains supplementary material, which is available to authorized users.
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spelling pubmed-43628362015-03-18 Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor Romanov, Michael N Farré, Marta Lithgow, Pamela E Fowler, Katie E Skinner, Benjamin M O’Connor, Rebecca Fonseka, Gothami Backström, Niclas Matsuda, Yoichi Nishida, Chizuko Houde, Peter Jarvis, Erich D Ellegren, Hans Burt, David W Larkin, Denis M Griffin, Darren K BMC Genomics Research Article BACKGROUND: The availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative molecular cytogenetics of only the largest chromosomes. Here, novel whole genome sequence information from 21 avian genome sequences (most newly assembled) made available on an interactive browser (Evolution Highway) was analyzed. RESULTS: Focusing on the six best-assembled genomes allowed us to assemble a putative karyotype of the dinosaur ancestor for each chromosome. Reconstructing evolutionary events that led to each species’ genome organization, we determined that the fastest rate of change occurred in the zebra finch and budgerigar, consistent with rapid speciation events in the Passeriformes and Psittaciformes. Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace. Analyzing chicken and zebra finch, we found little evidence to support the hypothesis of an association of evolutionary breakpoint regions with recombination hotspots but some evidence to support the hypothesis that microchromosomes largely represent conserved blocks of synteny in the majority of the 21 species analyzed. All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count. Ostrich, however, appeared to retain an overall karyotype structure of 2n = 80 despite undergoing a large number (26) of hitherto un-described interchromosomal changes. CONCLUSIONS: Results suggest that mechanisms exist to preserve a static overall avian karyotype/genomic structure, including the microchromosomes, with widespread interchromosomal change occurring rarely (e.g., in ostrich and budgerigar lineages). Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1060) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-11 /pmc/articles/PMC4362836/ /pubmed/25496766 http://dx.doi.org/10.1186/1471-2164-15-1060 Text en © Romanov 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
Romanov, Michael N
Farré, Marta
Lithgow, Pamela E
Fowler, Katie E
Skinner, Benjamin M
O’Connor, Rebecca
Fonseka, Gothami
Backström, Niclas
Matsuda, Yoichi
Nishida, Chizuko
Houde, Peter
Jarvis, Erich D
Ellegren, Hans
Burt, David W
Larkin, Denis M
Griffin, Darren K
Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title_full Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title_fullStr Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title_full_unstemmed Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title_short Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
title_sort reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4362836/
https://www.ncbi.nlm.nih.gov/pubmed/25496766
http://dx.doi.org/10.1186/1471-2164-15-1060
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