Skip to main content
Log in

Highly repetitive DNA families restricted to germ cells in a Japanese hagfish (Eptatretus burgeri): a hierarchical and mosaic structure in eliminated chromosomes

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

It is known that in eight hagfishes chromosome elimination occurs during early embryogenesis. The eliminated chromosomes are mostly C-band positive, so that none of the somatic cells have any C-band-positive chromatin. Recently, some highly repetitive DNA sequences have been reported as eliminated elements in these hagfishes based on molecular biological methods. However, no germline-restricted repetitive DNA have been directly isolated from the Japanese hagfish Eptatretus burgeri, from which approximately 21% of the total DNA is eliminated from presumptive somatic cells. Through electrophoretic investigation after digestion with restriction endonucleases, two DNA families that are restricted to germline DNA were isolated. Molecular cloning and sequence analysis revealed that these families are composed of closely related sequences of 64 and 57 bp in length, respectively. Southern blot hybridization revealed that the two DNA families are restricted to germline DNA and were thus named EEEb1 and EEEb2, respectively. Moreover, these eliminated elements were highly and tandemly repeated, and it is predicted that they might amplify by saltatory replication and have evolved in a concerted manner. By densitometric scanning, EEEb1 and EEEb2 were found to amount to make up approximately 18.5 and 0.024% of the total germline genomic DNA, accounting for 88.6% of the total eliminated DNA. A fluorescence in situ hybridization experiment demonstrated that EEEb1 is located on all C-band-positive chromosomes that are limited to germ cells, suggesting that EEEb1 is the primary component of eliminated DNA of E. burgeri.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bachmann, L., F. Venazetti & V. Sbordoni, 1996. Tandemly repeated satellite DNA of Dolichopoda schiavazzii: a test for models on the evolution of highly repetitive DNA. J. Mol. Evol. 43: 135–144.

    Google Scholar 

  • Baltimore, D., 1981. Gene conversion: some implications for immunoglobulin genes. Cell 24: 592–594.

    Google Scholar 

  • Basten, C.J. & T. Ohta, 1992. Simulation study of a multigene family, with special reference to the evolution of compensatory advantageous mutations. Genetics 132: 247–252.

    Google Scholar 

  • Boveri, T., 1887. Uber Differenzierung der Zellkerne wahrend der Furchung des Eies von Ascaris megalocephala. Anat. Anz. 2: 688–693.

    Google Scholar 

  • Britten, R.J. & D.E. Kohne, 1968. Repeated sequences in DNA. Science 161: 529–540.

    Google Scholar 

  • Dover, G.A., 1982. Molecular drive: a cohesive mode of species evolution. Nature 289: 111–117.

    Google Scholar 

  • Dover, G.A. & D. Tautz, 1986. Conversion and divergence in multigene families: alternatives to selection and drift. Philos. Trans. R. Soc. Lond. Ser. B 312: 275–289.

    Google Scholar 

  • Elder, J.F. & B.J. Turner, 1995. Concerted evolution of repetitive DNA sequences in eukaryotes. Q. Rev. Biol. 70: 297–320.

    Google Scholar 

  • Fan, Q. & M.-C. Yao, 2000. A lomg stringent sequence signal for programmed chromosome breakage in Tetrahymena thermophila. Nucl. Acids Res. 28: 895–900.

    Google Scholar 

  • Goday, C. & S. Pimpinelli, 1993. The occurrence, role and evolution of chromatin diminution in Nematodes. Parasitol Today 9: 319–322.

    Google Scholar 

  • Goto, Y., S. Kubota & S. Kohno, 1998. Highly repetitive DNA sequences that are restricted to the germ line in the hagfish Eptatretus cirrhatus: a mosaic of eliminated elements. Chromosoma 107: 17–32.

    Google Scholar 

  • John, B. & G.L.G. Miklos, 1979. Function aspects of satellite DNA and heterochromatin. Int. Rev. Cytogenet. Cell Genet. 41: 209–214.

    Google Scholar 

  • Kohno, S., Y. Nakai, S. Satoh, M. Yoshida & H. Kobayashi, 1986. Chromosome elimination in Japanese hagfish, Eptatretus burgeri (Agnatha, Cyclostomata). Cytogenet. Cell Genet. 41: 209–214.

    Google Scholar 

  • Kohno, S., S. Kubota & Y. Nakai, 1998. Chromatin diminution and chromosome elimination in hagfish species, pp. 81–100 in The Biology of Hagfishes, edited by J.M. Jørgensen, J.P. Lomholt, R.E. Weber & H. Malte. Chapman and Hall, London.

    Google Scholar 

  • Kubota, S., M. Kuro-o, S. Mizuno & S. Kohno, 1993. Germ line-restricted, highly repeated DNA sequences and their chromosomal localization in a Japanese hagfish (Eptatretus okinoseanus). Chromosoma 102: 163–173.

    Google Scholar 

  • Kubota, S., T. Ishibashi & S. Kohno, 1997. A germline restricted, highly repetitive DNA sequence in Paramyxine atami: an interspecifically conserved, but somatically eliminated, element. Mol. Gen. Genet. 256: 252–256.

    Google Scholar 

  • Linares, A.R., T. Bowen & G.A. Dover, 1994. Aspects of nonrandom turnover involved in the concerted evolution of intergenic spacers within the ribosomal DNA of Drosophila melanogaster. J. Mol. Evol. 39: 151–159.

    Google Scholar 

  • Müller, F., P. Walker, P. Aeby, H. Neuhaus, H. Felder, E. Back & H. Tobler, 1982. Nucleotide sequence of satellite DNA sequence contained in the eliminated genome of Ascaris lumbricoides. Nucl. Acids Res. 10: 7493–7510.

    Google Scholar 

  • Müller, F., C. Wicky, A. Spicher & H. Tobler, 1991. New telomere formation after developmentally regulated chromosomal breakage during process of chromatin diminution in Ascaris lumbricoides. Cell 67: 815–822.

    Google Scholar 

  • Nabeyama, M., S. Kubota & S. Kohno, 2000. Concerted evolution of a highly repetitive DNA family in Eptatretidae (Cyclostomata, Agnatha) implies specifically differential homogenization and amplification events in their germ cells. J. Mol. Evol. 50: 154–169.

    Google Scholar 

  • Nagylaki, T., 1984. The evolution of multigene families under intrachromosomal gene conversion. Genetics 106: 529–548.

    Google Scholar 

  • Nakai, Y., S. Kubota & S. Kohno, 1991. Chromatin diminution and chromosome elimination in four Japanese hagfish species. Cytogenet. Cell. Genet. 56: 196–198.

    Google Scholar 

  • Nakai, Y., S. Kobota, Y. Goto, T. Ishibashi, W. Davison & S. Kohno, 1995. Chromosome elimination in three Baltic, south Pacific and north-east Pacific hagfish species. Chrom. Res. 3: 321–330.

    Google Scholar 

  • Niedermaier, J. & K.B. Moritz, 2000. Organization and dynamics of satellite and telomere DNAs in Ascaris: implications for formation and programmed breakdown of compound chromosomes. Chromosoma 109: 439–452.

    Google Scholar 

  • Nowak, R., 1994. Mining treasures from ‘junk DNA'. Science 263: 608–610.

    Google Scholar 

  • Ohta, T., 1990. How gene families evolve. Theor. Popul. Biol. 37: 213–219.

    Google Scholar 

  • Ojima, Y., 1983. Fish Cytogenetics (in Japanese). Suikohsha, Tokyo.

  • Shichiri, M., Y. Kikuma, C.-H. Kuo, L.-L. Liu, S. Kubota & S. Kohno, 1997. Chromosome elimination and germ line-restricted microchromosomes in Paramyxine sheni from Taiwan. Chrom. Sci. 1: 49–53.

    Google Scholar 

  • Singer, M.F., 1982. Highly repeated sequences in mammalian genomes. Int. Rev. Cytol. 76: 67–112.

    Google Scholar 

  • Smith, G.P., 1976. Evolution of repeated DNA sequences by unequal crossover. Science 191: 528–535.

    Google Scholar 

  • Southern, E.M., 1970. Base sequence and evolution of guinea pig satellite DNA. Nature 227: 794–798.

    Google Scholar 

  • Staiber, W., I. Wech & A. Preiss, 1997. Isolation and chromosomal localization of a germ line-specific highly repetitive DNA family in Acricotopus lucidus (Diptera, Chironomidae). Chromosoma 106: 267–275.

    Google Scholar 

  • Streeck, R.E., K.B. Moritz & K. Beer, 1982. Chromatin diminution in Ascaris suum: nucleotide sequence of the eliminated satellite DNA. Nucl. Acids Res. 10: 3495–3502.

    Google Scholar 

  • Teschke, C., G. Solleder & K.B. Moritz, 1991. The highly variable pentameric repeats of the AT-rich germline limited DNA in Parascaris univalens are the telomeric repeats of somatic chromosomes. Nucl. Acids Res. 19: 2677–2684.

    Google Scholar 

  • Tobler, H., 1986. The differentiation of germ and somatic cell lines in Nematodes, pp. 1–69 in Germ Line-soma Differentiation. Results and Problems in Cell Differentiation, Vol. 13, edited by W. Hennig. Springer, Berlin, Heidelberg.

    Google Scholar 

  • Tobler, H., K.D. Smith & H. Ursprung, 1972. Molecular aspect of chromatin elimination in Ascaris lumbricoides. Dev. Biol. 27: 190–203.

    Google Scholar 

  • Tobler, H., A. Etter & F. Müller, 1992. Chromatin diminution in nematode development. Trends Genet. 8: 427–431.

    Google Scholar 

  • Vieira, J. & J. Messing, 1987. Production of single-stranded plasmid DNA. Methods Enzymol. 153: 3–11.

    Google Scholar 

  • Vogt, P., 1990. Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved ‘chromatin folding code'. Hum. Genet. 84: 301–336.

    Google Scholar 

  • Yao, M.-C., K. Zheng & C.-H. Yao, 1987. A conserved nucleotide sequence at the sites of developmentally regulated chromosome breakage in Tetrahymena. Cell 48: 779–788.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kubota, S., Takano, Ji., Tsuneishi, R. et al. Highly repetitive DNA families restricted to germ cells in a Japanese hagfish (Eptatretus burgeri): a hierarchical and mosaic structure in eliminated chromosomes. Genetica 111, 319–328 (2001). https://doi.org/10.1023/A:1013751600787

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1013751600787

Navigation