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Chromosome homologies of the highly rearranged karyotypes of four Akodon species (Rodentia, Cricetidae) resolved by reciprocal chromosome painting: the evolution of the lowest diploid number in rodents

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Abstract

Traditionally comparative cytogenetic studies are based mainly on banding patterns. Nevertheless, when dealing with species with highly rearranged genomes, as in Akodon species, or with other highly divergent species, cytogenetic comparisons of banding patterns prove inadequate. Hence, comparative chromosome painting has become the method of choice for genome comparisons at the cytogenetic level since it allows complete chromosome probes of a species to be hybridized in situ onto chromosomes of other species, detecting homologous genomic regions between them. In the present study, we have explored the highly rearranged complements of the Akodon species using reciprocal chromosome painting through species-specific chromosome probes obtained by chromosome sorting. The results revealed complete homology among the complements of Akodon sp. n. (ASP), 2n = 10; Akodon cursor (ACU), 2n = 15; Akodon montensis (AMO), 2n = 24; and Akodon paranaensis (APA), 2n = 44, and extensive chromosome rearrangements have been detected within the species with high precision. Robertsonian and tandem rearrangements, pericentric inversions and/or centromere repositioning, paracentric inversion, translocations, insertions, and breakpoints, where chromosomal rearrangements, seen to be favorable, were observed. Chromosome painting using the APA set of 21 autosomes plus X and Y revealed eight syntenic segments that are shared with A. montensis, A. cursor, and ASP, and one syntenic segment shared by A. montensis and A. cursor plus five exclusive chromosome associations for A. cursor and six for ASP chromosome X, except for the heterochromatin region of ASP X, and even chromosome Y shared complete homology among the species. These data indicate that all those closely related species have experienced a recent extensive process of autosomal rearrangement in which, except for ASP, there is still complete conservation of sex chromosomes homologies.

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Abbreviations

ACU:

Akodon cursor

AMO:

Akodon montensis

APA:

Akodon paranaensis

ASP:

Akodon sp. n.

DOP-PCR:

Degenerate oligonucleotide-primed PCR

FISH:

Fluorescent in situ hybridization

FN:

Fundamental number of autosomal arms

ITS:

Interstitial telomeric sequences

PCR:

Polymerase chain reaction

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Acknowledgements

We thank Dr. Willem Rens, Margaret Wallduck, Frances Lovell, and Laura Hirst for the valuable contributions during the lab work and data analysis. We also thank Dr. Maria José de Jesus Silva and Dr. Valéria Fagundes for the Akodon sp. n., A. cursor and A. montensis G-banding karyotypes and Silvia Sousa da Costa for technical assistance with the cell cultures. Permit for cell lines transportation was provided by IBAMA. Grants were received from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de do Amparo à Pesquisa Estado de São Paulo (FAPESP). The Cambridge Resource Center for Comparative Genomics was supported by a grant to MAFS from the Wellcome Trust.

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Authors and Affiliations

  1. Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, CEP 05508-900, São Paulo, São Paulo, Brazil

    Karen Ventura & Yatiyo Yonenaga-Yassuda

  2. Cambridge Resource Center for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 OES, UK

    Karen Ventura, Patricia C. M. O’Brien & Malcolm A. Ferguson-Smith

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  1. Karen Ventura
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  2. Patricia C. M. O’Brien
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  3. Yatiyo Yonenaga-Yassuda
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  4. Malcolm A. Ferguson-Smith
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Correspondence to Karen Ventura.

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Responsible Editor: Fengtang Yang.

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Ventura, K., O’Brien, P.C.M., Yonenaga-Yassuda, Y. et al. Chromosome homologies of the highly rearranged karyotypes of four Akodon species (Rodentia, Cricetidae) resolved by reciprocal chromosome painting: the evolution of the lowest diploid number in rodents. Chromosome Res 17, 1063–1078 (2009). https://doi.org/10.1007/s10577-009-9083-5

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  • DOI: https://doi.org/10.1007/s10577-009-9083-5

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