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The germ-line-restricted chromosome in the zebra finch: recombination in females and elimination in males

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Abstract

In the zebra finch (Taeniopygia guttata), there is a germ-line-restricted chromosome regularly present in males and females. A reexamination of male and female meiosis in the zebra finch showed that this element forms a euchromatic bivalent in oocytes, but it is always a single, heterochromatic element in spermatocytes. Immunostaining with anti-MLH1 showed that the bivalent in oocytes has two or three foci with a localized pattern, indicating the regular occurrence of recombination. In male meiosis, the single restricted chromosome forms an axis that contains the cohesin subunit SMC3, and the associated chromatin is densely packed until late pachytene. Electron microscopy of thin-sectioned seminiferous tubules shows that the restricted chromosome is eliminated in postmeiotic stages in the form of packed chromatin inside a micronucleus, visible in the cytoplasm of young spermatids. The selective condensation of the restricted chromosome during early meiotic prophase in males is interpreted as a strategy to avoid the triggering of asynaptic checkpoints, but this condensation is reversed prior to the final condensation that leads to its (ulterior) elimination. Recombination during female meiosis may prevent the genetic attrition of the restricted chromosome and, along with the elimination in male germ cells, ensures its regular transmission through females.

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References

  • Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetcis 151:1569–1579

    PubMed  CAS  Google Scholar 

  • Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A, Ashley T, Liskay RM (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336–342

    Article  PubMed  CAS  Google Scholar 

  • Barlow AL, Hulten MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6:350–358

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281:1986–1990

    Article  PubMed  CAS  Google Scholar 

  • Catalan J, Autio K, Kuosma E, Norppa H (1998) Age-dependent inclusion of sex chromosomes in lymphocyte micronuclei of man. Am J Hum Genet 63:1464–1472

    Article  PubMed  CAS  Google Scholar 

  • Christidis L (1986) Chromosomal evolution within the family Estrildidae (Aves). I. The Poephilae. Genetica 71:81–97

    Article  Google Scholar 

  • Cimini D, Fioravanti D, Salmon ED, Degrassi F (2002) Merotelic kinetochore orientation versus chromosome mono-orientation in the origin of lagging chromosomes in human primary cells. J Cell Sci 115:507–515

    PubMed  CAS  Google Scholar 

  • Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1β and SMC3. J Cell Biol 160:657–670

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756

    PubMed  CAS  Google Scholar 

  • Goday C, Esteban MR (2001) Chromosome elimination in sciarid flies. Bioessays 23:242–250

    Article  PubMed  CAS  Google Scholar 

  • Haig J (1978) The accumulation of deleterious genes in a population—Muller's ratchet. Theor Popul Biol 14:251–267

    Article  Google Scholar 

  • Hayman DL, Martin PG (1974) Mammalia I: Monotremata and Marsupialia. In: John B (ed) Animal cytogenetics 4: Chordata. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Hennig W (1986) Heterochromatin and germ line-restricted DNA. Results Probl Cell Differ 13:175–192

    PubMed  CAS  Google Scholar 

  • Itoh Y, Arnold AP (2005) Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56

    Article  PubMed  CAS  Google Scholar 

  • Jessberger R (2002) The many functions of SMC proteins in chromosome dynamics. Nat Rev Mol Cell Biol 3:767–778

    Article  PubMed  CAS  Google Scholar 

  • Jones RN, Rees H (1982) B chromosomes. Academic Press, London

    Google Scholar 

  • Kloc M, Zagrodzinska B (2001) Chromatin elimination—an oddity or a common mechanism in differentiation and development? Differentiation 68:84–91

    Article  PubMed  CAS  Google Scholar 

  • Kubota S, Takano J, Tsuneishi R, Kobayakawa S, Fujikawa N, Nabeyama M, Kohno S (2001) 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nasmyth K (2001) Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 35:673–745

    Article  PubMed  CAS  Google Scholar 

  • Nicklas RB (1997) How cells get the right chromosomes. Science 275:632–637

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Cell Genet 95:129–133

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1998) Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch, Taeniopygia guttata. Chromosome Res 6:105–113

    Article  PubMed  CAS  Google Scholar 

  • Pimpinelli S, Goday C (1989) Unusual kinetochores and chromatin diminution in Parascaris. Trends Genet 5:310–315

    Article  PubMed  CAS  Google Scholar 

  • Rice WR, Chippindale AK (2001) Sexual recombination and the power of natural selection. Science 294:555–559

    Article  PubMed  CAS  Google Scholar 

  • Roeder GS, Bailis JM (2000) The pachytene checkpoint. Trends Genet 16:395–403

    Article  PubMed  CAS  Google Scholar 

  • Solari AJ (1977) Ultrastructure of the synaptic autosomes and the ZW bivalent in chicken oocytes. Chromosoma 64:155–165

    Article  Google Scholar 

  • Solari AJ (1998) Structural analysis of meiotic chromosomes and synaptonemal complexes in higher vertebrates. In: Berrios M (ed) Nuclear structure and function. Academic, New York, pp 236–256

    Google Scholar 

  • Staiber W, Schiffkowski C (2000) Structural evolution of the germ line-limited chromosomes in Acricotopus. Chromosoma 109:343–349

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takagi N (1972) A comparative study of the chromatin replication in 6 species of birds. Jap J Genetics 47:115–123

    Google Scholar 

  • Tarsounas M, Moens PB (2001) Checkpoint and DNA-repair proteins are associated with the cores of mammalian meiotic chromosomes. Curr Top Dev Biol 51:109–134

    Article  PubMed  CAS  Google Scholar 

  • Tiersch TR, Wachtel SS (1991) On the evolution of genome size in birds. J Hered 82:363–368

    PubMed  CAS  Google Scholar 

  • White MJD (1973) Animal cytology and evolution. Cambridge University Press, Cambridge, UK

    Google Scholar 

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Acknowledgements

The kind gifts of anti-SCP3 from P. Moens and CREST serum from W. Brinkley are gratefully acknowledged. The able technical help of C. Deparci is thanked. This work was supported by grants from the National Research Council (CONICET) and National Agency for Science and Technology. AJS and MIP are researchers from CONICET.

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Correspondence to M. I. Pigozzi.

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Communicated by P. Moens

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Pigozzi, M.I., Solari, A.J. The germ-line-restricted chromosome in the zebra finch: recombination in females and elimination in males. Chromosoma 114, 403–409 (2005). https://doi.org/10.1007/s00412-005-0025-5

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  • DOI: https://doi.org/10.1007/s00412-005-0025-5

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