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Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes

BACKGROUND: Previous cross-species painting studies with probes from chicken (Gallus gallus) chromosomes 1–10 and a paint pool of nineteen microchromosomes have revealed that the drastic karyotypic reorganization in Accipitridae is due to extensive synteny disruptions and associations. However, the...

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Autores principales: Nie, Wenhui, O’Brien, Patricia C. M., Fu, Beiyuan, Wang, Jinghuan, Su, Weiting, He, Kai, Bed’Hom, Bertrand, Volobouev, Vitaly, Ferguson-Smith, Malcolm A., Dobigny, Gauthier, Yang, Fengtang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4583764/
https://www.ncbi.nlm.nih.gov/pubmed/26409465
http://dx.doi.org/10.1186/s12862-015-0484-0
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author Nie, Wenhui
O’Brien, Patricia C. M.
Fu, Beiyuan
Wang, Jinghuan
Su, Weiting
He, Kai
Bed’Hom, Bertrand
Volobouev, Vitaly
Ferguson-Smith, Malcolm A.
Dobigny, Gauthier
Yang, Fengtang
author_facet Nie, Wenhui
O’Brien, Patricia C. M.
Fu, Beiyuan
Wang, Jinghuan
Su, Weiting
He, Kai
Bed’Hom, Bertrand
Volobouev, Vitaly
Ferguson-Smith, Malcolm A.
Dobigny, Gauthier
Yang, Fengtang
author_sort Nie, Wenhui
collection PubMed
description BACKGROUND: Previous cross-species painting studies with probes from chicken (Gallus gallus) chromosomes 1–10 and a paint pool of nineteen microchromosomes have revealed that the drastic karyotypic reorganization in Accipitridae is due to extensive synteny disruptions and associations. However, the number of synteny association events and identities of microchromosomes involved in such synteny associations remain undefined, due to the lack of paint probes derived from individual chicken microchromosomes. Moreover, no genome-wide homology map between Accipitridae species and other avian species with atypical karyotype organization has been reported till now, and the karyotype evolution within Accipitriformes remains unclear. RESULTS: To delineate the synteny-conserved segments in Accipitridae, a set of painting probes for the griffon vulture, Gyps fulvus (2n = 66) was generated from flow-sorted chromosomes. Together with previous generated probes from the stone curlew, Burhinus oedicnemus (2n = 42), a Charadriiformes species with atypical karyotype organization, we conducted multidirectional chromosome painting, including reciprocal chromosome painting between B. oedicnemus and G. fulvus and cross-species chromosome painting between B. oedicnemus and two accipitrid species (the Himalayan griffon, G. himalayensis 2n = 66, and the common buzzard, Buteo buteo, 2n = 68). In doing so, genome-wide homology maps between B. oedicnemus and three Accipitridae species were established. From there, a cladistic analysis using chromosomal characters and mapping of chromosomal changes on a consensus molecular phylogeny were conducted in order to search for cytogenetic signatures for different lineages within Accipitriformes. CONCLUSION: Our study confirmed that the genomes of the diurnal birds of prey, especially the genomes of species in Accipitriformes excluding Cathartidae, have been extensively reshuffled when compared to other bird lineages. The chromosomal rearrangements involved include both fusions and fissions. Our chromosome painting data indicated that the Palearctic common buzzard (BBU) shared several common chromosomal rearrangements with some Old World vultures, and was found to be more closely related to other Accipitridae than to Neotropical buteonine raptors from the karyotypic perspective. Using both a chromosome-based cladistic analysis as well as by mapping of chromosomal differences onto a molecular-based phylogenetic tree, we revealed a number of potential cytogenetic signatures that support the clade of Pandionidae (PHA) + Accipitridae. In addition, our cladistic analysis using chromosomal characters appears to support the placement of osprey (PHA) in Accipitridae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0484-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-45837642015-09-27 Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes Nie, Wenhui O’Brien, Patricia C. M. Fu, Beiyuan Wang, Jinghuan Su, Weiting He, Kai Bed’Hom, Bertrand Volobouev, Vitaly Ferguson-Smith, Malcolm A. Dobigny, Gauthier Yang, Fengtang BMC Evol Biol Research Article BACKGROUND: Previous cross-species painting studies with probes from chicken (Gallus gallus) chromosomes 1–10 and a paint pool of nineteen microchromosomes have revealed that the drastic karyotypic reorganization in Accipitridae is due to extensive synteny disruptions and associations. However, the number of synteny association events and identities of microchromosomes involved in such synteny associations remain undefined, due to the lack of paint probes derived from individual chicken microchromosomes. Moreover, no genome-wide homology map between Accipitridae species and other avian species with atypical karyotype organization has been reported till now, and the karyotype evolution within Accipitriformes remains unclear. RESULTS: To delineate the synteny-conserved segments in Accipitridae, a set of painting probes for the griffon vulture, Gyps fulvus (2n = 66) was generated from flow-sorted chromosomes. Together with previous generated probes from the stone curlew, Burhinus oedicnemus (2n = 42), a Charadriiformes species with atypical karyotype organization, we conducted multidirectional chromosome painting, including reciprocal chromosome painting between B. oedicnemus and G. fulvus and cross-species chromosome painting between B. oedicnemus and two accipitrid species (the Himalayan griffon, G. himalayensis 2n = 66, and the common buzzard, Buteo buteo, 2n = 68). In doing so, genome-wide homology maps between B. oedicnemus and three Accipitridae species were established. From there, a cladistic analysis using chromosomal characters and mapping of chromosomal changes on a consensus molecular phylogeny were conducted in order to search for cytogenetic signatures for different lineages within Accipitriformes. CONCLUSION: Our study confirmed that the genomes of the diurnal birds of prey, especially the genomes of species in Accipitriformes excluding Cathartidae, have been extensively reshuffled when compared to other bird lineages. The chromosomal rearrangements involved include both fusions and fissions. Our chromosome painting data indicated that the Palearctic common buzzard (BBU) shared several common chromosomal rearrangements with some Old World vultures, and was found to be more closely related to other Accipitridae than to Neotropical buteonine raptors from the karyotypic perspective. Using both a chromosome-based cladistic analysis as well as by mapping of chromosomal differences onto a molecular-based phylogenetic tree, we revealed a number of potential cytogenetic signatures that support the clade of Pandionidae (PHA) + Accipitridae. In addition, our cladistic analysis using chromosomal characters appears to support the placement of osprey (PHA) in Accipitridae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0484-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-26 /pmc/articles/PMC4583764/ /pubmed/26409465 http://dx.doi.org/10.1186/s12862-015-0484-0 Text en © Nie et al. 2015 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
Nie, Wenhui
O’Brien, Patricia C. M.
Fu, Beiyuan
Wang, Jinghuan
Su, Weiting
He, Kai
Bed’Hom, Bertrand
Volobouev, Vitaly
Ferguson-Smith, Malcolm A.
Dobigny, Gauthier
Yang, Fengtang
Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title_full Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title_fullStr Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title_full_unstemmed Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title_short Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes
title_sort multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within accipitriformes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4583764/
https://www.ncbi.nlm.nih.gov/pubmed/26409465
http://dx.doi.org/10.1186/s12862-015-0484-0
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