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Robertsonian fusions, pericentromeric repeat organization and evolution: a case study within a highly polymorphic rodent species, Gerbillus nigeriae

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Abstract

Pericentromeric repeats have been claimed to mediate centric fusions through heterologous recombination of arrays of tandemly repeated and highly homogenized motifs. However, mammalian case studies are essentially restricted to pathologic fusions in human, or to the house mouse Roberstonian (Rb) races. We here provide an example in a wild gerbil rodent, Gerbillus nigeriae, which displays an extensive Rb polymorphism, with 2n ranging between 2n = 60 and 74. The distribution of two closely related repeats, GERB1 and GERB2 that were previously isolated by Volobouev et al. (Chromosoma 104:252–259, 1995) in this African species, were investigated in the genomes of seven individuals with various diploid numbers. Our results clearly show that GERB1 and GERB2 are organized in a non-random manner, with GERB2 and GERB1 being clearly juxtacentromeric and centromeric, respectively. Finally, cloning and sequencing revealed that, unlike GERB2, GERB1 monomers display a more homogeneous organization at both the nucleotide and structural levels. Altogether, our results point toward a pivotal role of GERB1 repeats in the mediation of Rb fusions through heterologous recombination, with some evidence of subsequent loss of repeats after the Rb fusion during the course of evolution of metacentric elements. Moreover, the repeat pattern observed in G. nigeriae closely matches the organization and sequence structure of satellite DNAs described in human acrocentrics. Consequently, G. nigeriae appears as an additional model for the study of repeat evolution and its role in centric fusions and their consequences in mammals.

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Abbreviations

DAPI:

4′,6-diamino-2-phenylindole

FISH:

fluorescent in situ hybridization

FITC:

fluorescein isothiocyanate

LINE-1:

long interspersed element one

PCR:

polymerase chain reaction

PRINS:

primed in situ hybridization

Rb fusion:

Robertsonian fusion

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Acknowledgments

Ambroise Dalecky and Massamba Thiam kindly provided the gerbil samples from Mali and Senegal for cell culture purposes. Most of our survey, including field work in Niger, was funded by the IRD and the ANR (program no. ANR-05-JC05-48631 led by G. Dobigny). Work permit in the W National Park area was kindly provided by Mr Soumeïla Sahailou (coord. ECOPAS program). We would also like to thank the IFR119 “Montpellier Environnement Biodiversité” who partly funded some of the cell culture and fluorescence microscopy equipment used in this study. We are grateful to Janice Britton-Davidian for very helpful comments and stimulating discussions, as well as to Malcolm Ferguson-Smith and Herbert McGregor for their help with the English wording.

We wish to dedicate this work to our dear friend and colleague Adamou Nomao who spent 4 years working on G. nigeriae, but left us precociously.

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Authors and Affiliations

  1. Institut de Recherche pour le Développement, Centre de Biologie et de Gestion des Populations (CBGP; UMR022 IRD-INRA-Montpellier SupAgro), Campus International de Baillarguet, CS30016, 34988, Montferrier-sur-Lez, France

    Philippe Gauthier, Karmadine Hima & Gauthier Dobigny

  2. IRD, Centre Régional Agrhymet, Rive Droite, 11011, Niamey, Niger

    Karmadine Hima & Gauthier Dobigny

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  1. Philippe Gauthier
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  2. Karmadine Hima
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Correspondence to Gauthier Dobigny.

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Responsible Editor: Fentang Yang.

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Supplementary Figure

Sequence alignment of the four GERB1-containing clones (numbers 2–5) as well as Volobouev et al.’s (1995) one (number 1). For clarity, each clone was aligned following the motifs A–H (271 bp) substructure. See text and Fig. 5 for details. (PDF 190 kb)

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Gauthier, P., Hima, K. & Dobigny, G. Robertsonian fusions, pericentromeric repeat organization and evolution: a case study within a highly polymorphic rodent species, Gerbillus nigeriae . Chromosome Res 18, 473–486 (2010). https://doi.org/10.1007/s10577-010-9128-9

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