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The puzzling character of repetitive DNA in Phodopus genomes (Cricetidae, Rodentia)

Abstract

Three novel repetitive DNA sequences are described, presenting a similar heterochromatic chromosomal location in two hamster species: Phodopus roborovskii and Phodopus sungorus (Cricetidae, Rodentia). Namely, two species-specific repetitive sequences (PROsat from P. roborovskii and PSUchr1sat from P. sungorus) surrounding a third one (PsatDNA), that is shared by both hamster genomes. Fiber-FISH analyses revealed that PROsat intermingles with PsatDNA in P. roborovskii and PSUchr1sat intermingles with PsatDNA in P. sungorus. A model explaining the evolution of this intricate chromosomal distribution is proposed, which can explain better the evolution of these very derivative genomes (in comparison to the ancestral Muroidea). The most plausible evolutionary scenario seems to be the expansion of a number of repeats into other’s domain, most probably resulting in its intermingling, followed by the subsequent spread of these complex repeats from a single chromosomal location to other chromosomes. Evidences of an association between repetitive sequences and the chromosome evolution process were observed, namely for PROsat. Most probably, the evolutionary breakpoints that shaped PRO and PSU chromosomes (pericentric inversions and fusions) occurred within the boundaries of PROsat blocks in the ancestor. The repeats high diversity at the heterochromatic regions of Phodopus chromosomes, together with its complex organization, suggests that these species are important models for evolutionary studies, namely in the investigation of a possible relationship between repetitive sequences and the occurrence of chromosomal rearrangements and consequently, in genome evolution.

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Abbreviations

3′UTR:

3′ untranslated region

5′TAMRA:

5′ Carboxytetramethylrhodamine

APK:

Ancestral Phodopus Karyotype

BLAST:

Basic Local Alignment Search Tool

CBP-banding:

C-bands by barium hydroxide with propidium iodide

CCR:

Cricetus cricetus

EMBOSS:

European Molecular Biology Open Software Suite

Fiber-FISH:

FISH on stretched chromatin fibers

FISH:

fluorescent in situ hybridization

FITC:

fluorescein isothiocyanate

LINE-1:

long interspersed nuclear element-1

NCBI:

National Center for Biotechnology Information

ORF2:

open reading frame 2

PCR:

polymerase chain reaction

PER:

Peromyscus eremicus

PRO:

Phodopus roborovskii

PROsat:

Phodopus roborovskii satellite

PsatDNA:

Phodopus satellite DNA

PSU:

Phodopus sungorus

PSUchr1sat:

Phodopus sungorus chromosome 1 satellite

REs:

restriction enzymes

RNO:

Rattus norvegicus

SatDNAs:

Satellite DNAs

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Acknowledgments

This work was funded by the project POCI/BIA-BCM/58541/2004, a PhD grant (SFRH/BD/41574/2007), and a research position on Animal Genomics of the “Sistema Científico e Tecnológico Nacional—Ciência 2007”, all from the Science and Technology Foundation (FCT) from Portugal. We are deeply grateful to Dr. Vitaly Volobouev for providing the C. cricetus and P. eremicus cell cultures.

Compliance with Ethical Standards

This research is in agreement with the current laws of the country in which they were performed. This article does not contain any studies with human or animal subjects performed by the any of the authors. All the authors are in agreement to the submission of this manuscript to Chromosome Research.

Conflict of interest

All authors declare that they have no competing interests.

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Correspondence to Raquel Chaves.

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Responsible Editors: Maria Assunta Biscotti, Pat Heslop-Harrison and Ettore Olmo

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Paço, A., Adega, F., Meštrović, N. et al. The puzzling character of repetitive DNA in Phodopus genomes (Cricetidae, Rodentia). Chromosome Res 23, 427–440 (2015). https://doi.org/10.1007/s10577-015-9481-9

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Keywords

  • Rodentia
  • Phodopus
  • Repetitive sequences
  • Chromosomal evolution