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On the Origin and Evolution of the Extant System of B Chromosomes in Oryzomyini Radiation (Rodentia, Sigmodontinae).

Ventura K, O'Brien PC, do Nascimento Moreira C, Yonenaga-Yassuda Y, Ferguson-Smith MA - PLoS ONE (2015)

Bottom Line: The results reveal that among the species sampled, 12 of them, belonging to a monophyletic Oryzomiyini subclade, are positive for an anonymous Oryzomyini shared heterochromatic region (OSHR) on both sex chromosomes.The diversity of the Oryzomyini Bs in number, size, morphology and genetic content may be explained by the independent origin of B chromosomes in different subgroups of species, with Bs in Holochilus brasiliensis, Nectomys squamipes and N. rattus sharing the OSHR with sex chromosomes, and those in Oligoryzomys flavescens and Sooretamys angouya lacking OSHR in Bs.The species-specific pattern of Bs is probably a consequence of their independent evolutionary origin.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil; Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom; Instituto de Recursos Naturais - Universidade Federal de Itajubá, Itajubá, Minas Gerais, Brazil.

ABSTRACT
Heterogeneous supernumerary chromosomes (Bs) are recognized in the oryzomyines Holochilus brasiliensis, Nectomys rattus, N. squamipes, Oligoryzomys flavescens and Sooretamys angouya, representing about 10% of all known B-containing rodent species. They provide an outstanding model for understanding the origin, evolution and diversity of Bs in a phylogenetic context. Therefore, whole chromosome-specific probes were generated from flow-sorted Holochilus brasiliensis (HBR) autosomes 11 and 25+26 and chromosomes X, Y and Bs. Hybridizations were performed on male metaphases of 15 Oryzomyini species of which 3 are B-containing species. The results reveal that among the species sampled, 12 of them, belonging to a monophyletic Oryzomiyini subclade, are positive for an anonymous Oryzomyini shared heterochromatic region (OSHR) on both sex chromosomes. The OSHR is also present on Bs of Holochilus brasiliensis, Nectomys rattus and N. squamipes but not on Bs of O. flavescens and S. angouya. Two distinct additional OSHR/autosome associations are observed on S. angouya. The three species that are OSHR negative belong to an outgroup. Molecular dating suggests that the OSHR originated between 7.8 and 3 Mya on ancestral sex chromosomes. A tentative explanation for the OSHR-positive nature of B regions in three species could be that transposable elements (TEs) from this specific sex chromosome region may have invaded existing B chromosomes. The presence of the OSHR on entire Xp and Yp adjacent to interstitial telomeric sequences at pericentromeric positions, as observed in Drymoreomys albimaculatus, show a similar organization as on B chromosomes in Nectomys squamipes. The diversity of the Oryzomyini Bs in number, size, morphology and genetic content may be explained by the independent origin of B chromosomes in different subgroups of species, with Bs in Holochilus brasiliensis, Nectomys squamipes and N. rattus sharing the OSHR with sex chromosomes, and those in Oligoryzomys flavescens and Sooretamys angouya lacking OSHR in Bs. The species-specific pattern of Bs is probably a consequence of their independent evolutionary origin.

No MeSH data available.


Characterization of Drymoreomys albimaculatus X and Y, and Nectomys squamipes B after hybridization using HBR Y and telomeric sequences as probes (a) Sex chromosomes of a male Drymoreomys albimaculatus after dual-colour FISH. HBR Y signals are red and telomeric sequences are green. (b) Medium metacentric B of N. squamipes after dual-colour FISH. HBR Y signals are green and telomeric sequences are red. Note the pericentromeric ITS linked to OSHR on the X and Y chromosomes of D. albimaculatus and on N. squamipes supernumerary.
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pone.0136663.g006: Characterization of Drymoreomys albimaculatus X and Y, and Nectomys squamipes B after hybridization using HBR Y and telomeric sequences as probes (a) Sex chromosomes of a male Drymoreomys albimaculatus after dual-colour FISH. HBR Y signals are red and telomeric sequences are green. (b) Medium metacentric B of N. squamipes after dual-colour FISH. HBR Y signals are green and telomeric sequences are red. Note the pericentromeric ITS linked to OSHR on the X and Y chromosomes of D. albimaculatus and on N. squamipes supernumerary.

Mentions: (a) Whole HBR Y, HBR B1 and B2 and, region of HBR X painted by HBR Y probe; (b) Whole HBR X, HBR B1 and B2 and, region of HBR Y painted by HBR X probe. (c) Whole HBR B1 and B2, and regions of HBR Y and HBR X painted by HBR B1 or B2 probes. Painted chromosomes or regions are in pink.


On the Origin and Evolution of the Extant System of B Chromosomes in Oryzomyini Radiation (Rodentia, Sigmodontinae).

Ventura K, O'Brien PC, do Nascimento Moreira C, Yonenaga-Yassuda Y, Ferguson-Smith MA - PLoS ONE (2015)

Characterization of Drymoreomys albimaculatus X and Y, and Nectomys squamipes B after hybridization using HBR Y and telomeric sequences as probes (a) Sex chromosomes of a male Drymoreomys albimaculatus after dual-colour FISH. HBR Y signals are red and telomeric sequences are green. (b) Medium metacentric B of N. squamipes after dual-colour FISH. HBR Y signals are green and telomeric sequences are red. Note the pericentromeric ITS linked to OSHR on the X and Y chromosomes of D. albimaculatus and on N. squamipes supernumerary.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4549248&req=5

pone.0136663.g006: Characterization of Drymoreomys albimaculatus X and Y, and Nectomys squamipes B after hybridization using HBR Y and telomeric sequences as probes (a) Sex chromosomes of a male Drymoreomys albimaculatus after dual-colour FISH. HBR Y signals are red and telomeric sequences are green. (b) Medium metacentric B of N. squamipes after dual-colour FISH. HBR Y signals are green and telomeric sequences are red. Note the pericentromeric ITS linked to OSHR on the X and Y chromosomes of D. albimaculatus and on N. squamipes supernumerary.
Mentions: (a) Whole HBR Y, HBR B1 and B2 and, region of HBR X painted by HBR Y probe; (b) Whole HBR X, HBR B1 and B2 and, region of HBR Y painted by HBR X probe. (c) Whole HBR B1 and B2, and regions of HBR Y and HBR X painted by HBR B1 or B2 probes. Painted chromosomes or regions are in pink.

Bottom Line: The results reveal that among the species sampled, 12 of them, belonging to a monophyletic Oryzomiyini subclade, are positive for an anonymous Oryzomyini shared heterochromatic region (OSHR) on both sex chromosomes.The diversity of the Oryzomyini Bs in number, size, morphology and genetic content may be explained by the independent origin of B chromosomes in different subgroups of species, with Bs in Holochilus brasiliensis, Nectomys squamipes and N. rattus sharing the OSHR with sex chromosomes, and those in Oligoryzomys flavescens and Sooretamys angouya lacking OSHR in Bs.The species-specific pattern of Bs is probably a consequence of their independent evolutionary origin.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil; Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom; Instituto de Recursos Naturais - Universidade Federal de Itajubá, Itajubá, Minas Gerais, Brazil.

ABSTRACT
Heterogeneous supernumerary chromosomes (Bs) are recognized in the oryzomyines Holochilus brasiliensis, Nectomys rattus, N. squamipes, Oligoryzomys flavescens and Sooretamys angouya, representing about 10% of all known B-containing rodent species. They provide an outstanding model for understanding the origin, evolution and diversity of Bs in a phylogenetic context. Therefore, whole chromosome-specific probes were generated from flow-sorted Holochilus brasiliensis (HBR) autosomes 11 and 25+26 and chromosomes X, Y and Bs. Hybridizations were performed on male metaphases of 15 Oryzomyini species of which 3 are B-containing species. The results reveal that among the species sampled, 12 of them, belonging to a monophyletic Oryzomiyini subclade, are positive for an anonymous Oryzomyini shared heterochromatic region (OSHR) on both sex chromosomes. The OSHR is also present on Bs of Holochilus brasiliensis, Nectomys rattus and N. squamipes but not on Bs of O. flavescens and S. angouya. Two distinct additional OSHR/autosome associations are observed on S. angouya. The three species that are OSHR negative belong to an outgroup. Molecular dating suggests that the OSHR originated between 7.8 and 3 Mya on ancestral sex chromosomes. A tentative explanation for the OSHR-positive nature of B regions in three species could be that transposable elements (TEs) from this specific sex chromosome region may have invaded existing B chromosomes. The presence of the OSHR on entire Xp and Yp adjacent to interstitial telomeric sequences at pericentromeric positions, as observed in Drymoreomys albimaculatus, show a similar organization as on B chromosomes in Nectomys squamipes. The diversity of the Oryzomyini Bs in number, size, morphology and genetic content may be explained by the independent origin of B chromosomes in different subgroups of species, with Bs in Holochilus brasiliensis, Nectomys squamipes and N. rattus sharing the OSHR with sex chromosomes, and those in Oligoryzomys flavescens and Sooretamys angouya lacking OSHR in Bs. The species-specific pattern of Bs is probably a consequence of their independent evolutionary origin.

No MeSH data available.