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Chromosoma

, Volume 89, Issue 3, pp 169–185 | Cite as

Chromosome 1 in crested and marbled newts (Triturus)

An extraordinary case of heteromorphism and independent chromosome evolution
  • Simon H. Sims
  • Herbert C. Macgregor
  • Patricia S. Pellatt
  • Heather A. Horner
Article

Abstract

The heteromorphic chromosomes 1 of Triturus cristatus carnifex and T. marmoratus were studied in mitotic metaphase after staining with the Giemsa C-banding technique and with the fluorochromes, DAPI (AT-specific) and mithramycin (GC-specific). They were also examined in the lampbrush form under phase-contrast before fixation and after fixation and staining with Giemsa. Chromosomes 1 of T.c. carnifex are asynaptic and achiasmatic throughout most of their long arms. They are also heteromorphic in most of their long arms for the patterns of Giemsa and fluorochrome staining and the distribution of distinctive lampbrush loops. The heteromorphic regions correspond to the regions that are asynaptic and achiasmatic. They stain more strongly with mithramycin and more weakly with DAPI than the remainder of the chromosomes, signifying that their DNA is relatively rich in GC. The patterns of staining with Giemsa and fluorochromes and the distributions of distinctive lateral loops vary from one animal to another in the same species and even in the same population. The asynaptic and achiasmatic regions of chromosomes 1 in T. marmoratus extend throughout the whole of the long arms and well beyond the heterochromatic region. Chiasmata form only in the short arm and occasionally in the short euchromatic segment at the tip of the long arms. The staining patterns of chromosomes 1 in T. marmoratus differ from those in T.c. carnifex although, like carnifex, their DNA is relatively GC-rich. The chromosomes 1 of T. marmoratus are more submetacentric than those of T.c. carnifex. In T. marmoratus chromosome 1B is about 12% shorter than 1A. There is a short paracentric inversion heterozygosity in the long arm of chromosome 1B in T. marmoratus which probably accounts for the lack of chiasmata in the euchromatin that separates the centromere from the start of the heterochromatin. In both carnifex and marmoratus, embryos that are homomorphic for chromosome 1 arrest and die at the late tailbud stage of development. The same applies to F1 hybrid embryos T.c. carnifex x T. marmoratus, and this has permitted identification of chromosomes 1A and 1B in both species. There is no correspondence between patterns of Giemsa or fluorochrome staining of the heteromorphic regions of chromosome 1 and any feature of the lampbrush chromosomes. However, the short euchromatic ends of the long arms of chromosomes 1 in both species are distinguished in the lampbrush form by a series of uniformly small loops of fine texture associated with very small chromomeres. The Giemsa C-staining patterns of both chromosomes 1A and 1B are different in each of the four subspecies of T. cristatus. T.c. karelinii stands out by having unusually large masses of Giemsa C-staining centromeric heterochromatin on all but 1 of its 12 chromosomes. A scheme is proposed for the evolution of chromosome 1 in T. cristatus and T. marmoratus, based on all available cytological and molecular data.

Keywords

Mithramycin Lampbrush Chromosome Paracentric Inversion Tailbud Stage Heteromorphic Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Batistoni R, Nardi I, Barsacchi-Pilone G (1974) Banding patterns on lampbrush chromosomes of Triturus marmoratus (Amphibia Urodela) by the Giemsa stain. Chromosoma 49:121–134Google Scholar
  2. Behr W, Honikel K, Hartmann G (1969) Interaction of the RNA polymerase inhibitor chromomycin with DNA. Eur J Biochem 9:82–92Google Scholar
  3. Burkholder GD, Duczek LL (1980) Proteins in chromosome banding. II. Effect of Rand C-banding treatments on the proteins of isolated nuclei. Chromosoma 79:43–51Google Scholar
  4. Callan HG, Lloyd L (1960) Lampbrush chromosomes of crested newts Triturus cristatus (Laurenti). Phil Trans R Soc Lond B 243:134–219Google Scholar
  5. Callan HG, Lloyd L (1975) Working maps of the lampbrush chromosomes of Amphibia. In: King RC (ed) Handbook of genetics, vol 4. Plenum Publishing Corp, New York, pp 57–77Google Scholar
  6. Comings DE (1975) Mechanisms of chromosome banding. VIII. Hoechst 33258-DNA interaction. Chromosoma 52:229–243Google Scholar
  7. Comings DE, Avelino E, Okada TA, Wyandt HE (1973) The mechanism of C- and G-banding of chromosomes. Exp Cell Res 77:469–493Google Scholar
  8. Conger AD, Fairchild LM (1953) A quick-freeze method for making smear slides permanent. Stain Technol 28:281–283Google Scholar
  9. Estes R, Hoffstetter R (1976) Les urodels du Miocene de la GriveSaint-Alban (Isère, France). Bull Mus Nat Hist Paris, sér 3 (Sciences de la terre 57), (398): 297–343Google Scholar
  10. Hecht MK, Hoffstetter R (1962) Note préliminaire sur les Amphibiens et les Squamates du Landénien superieur et du Tongrien de belgique. Bull Inst Roy Scienc Nat 38:1–30Google Scholar
  11. Horner HA, Macgregor HC (1984) Normal development in crested newts (Triturus) and its arrest as a consequence of an unusual chromosomal situation. J Herpetol (in press)Google Scholar
  12. Kezer J, Macgregor HC (1971) A fresh look at meiosis and centromeric heterochromatin in the red-backed salamander Plethodon cinereus cinereus (Green). Chromosoma 33:146–166Google Scholar
  13. Lin MS, Comings DE, Alfi OS (1977) Optical studies of the interaction of 4′, 6-diamidino-2-phenylindole with DNA and metaphase chromosomes. Chromosoma 60:15–26Google Scholar
  14. Macgregor HC (1979) In situ hybridization of highly repetitive DNA to chromosomes of Triturus cristatus. Chromosoma 71:57–64Google Scholar
  15. Macgregor HC, Andrews C (1977) The arrangement and transcription of “middle repetitive” DNA sequences on lampbrush chromosomes of Triturus. Chromosoma 63:109–126Google Scholar
  16. Macgregor HC, Callan HG (1962) The actions of enzymes on lampbrush chromosomes. Quart J Micr Sci 103:173–203Google Scholar
  17. Macgregor HC, Horner HA (1980) Heteromorphism for chromosome 1, a requirement for normal development in crested newts. Chromosoma 76:111–122Google Scholar
  18. Macgregor HC, Varley JM (1983) Working with animal chromosomes. John Wiley and Sons, Chichester (England) and New YorkGoogle Scholar
  19. Macgregor HC, Horner HA, Owen CA, Parker I (1973) Observations on centromeric heterochromatin and satellite DNA in salamanders of the genus Plethodon. Chromosoma 43:329–384Google Scholar
  20. Macgregor HC, Varley JM, Morgan GT (1981) The transcription of satellite and ribosomal DNA sequences on lampbrush chromosomes of crested newts. In: Schweiger HG (ed) International cell biology 1980–81. Springer, Berlin Heidelberg, pp 33–46Google Scholar
  21. Macgregor HC, Horner HA, Sims SH (1983) Newt chromosomes and some problems in evolutionary cytogenetics. In: Kew chromosome conference II. George, Allen and Unwin, London, pp 283–294Google Scholar
  22. Mancino G, Nardi I (1971) Chromosomal heteromorphism and female heterogamety in the marbled newt Triturus marmoratus (Latreille, 1800). Experientia 27:821–822Google Scholar
  23. Mancino G, Ragghianti M, Bucci-Innocenti SB (1973) I cariotipi di Triturus marmoratus e T. cristatus studiati con il “C-staining method”. Rend Acc Naz Lincei 55:559–564Google Scholar
  24. Mancino G, Ragghianti M, Bucci-Innocenti S (1977) Cytotaxonomy and cytogenetics in European newt species. In: Taylor DH, Guttman SI (eds) The reproductive biology of amphibians. Plenum Publishing Corp, New York, pp 411–447Google Scholar
  25. Morgan GT (1978) Absence of chiasmata from the heteromorphic region of chromosome 1 during spermatogenesis in Triturus cristatus carnifex. Chromosoma 66:269–280Google Scholar
  26. Morgan GT, Macgregor HC, Coleman A (1980) Multiple ribosomal gene sites revealed by in situ hybridization of Xenopus rDNA to Triturus lampbrush chromosomes. Chromosoma 80:309–330Google Scholar
  27. Müller W, Crothers DM (1975) Interactions of heteroaromatic compounds with nucleic acids. 1. The influence of heteroatoms and polarizability on the base specificity of intercalating ligands. Eur J Biochem 54:267–277Google Scholar
  28. Müller W, Gautier F (1975) Interactions of heteroaromatic compounds with nucleic acids. AT-specific non-intercalating DNA ligands. Eur J Biochem 54:385–394Google Scholar
  29. Nardi I, Ragghianti M, Mancino G (1972) Characterization of the lampbrush chromosomes of the marbled newt Triturus marmoratus (Latreille, 1800). Chromosoma 37:1–22Google Scholar
  30. Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis (Daudin). Second edition. North-Holland Publishing Company, AmsterdamGoogle Scholar
  31. Sanchíz Fd-B, Mlynarski M (1979) Pliocene salamandrids (Amphibia, Caudata) from Poland. Acta Zool Cracov 24:175–188Google Scholar
  32. Scheer U, Franke WW, Trendelenburg MF, Spring H (1976) Classification of loops of lampbrush chromosomes according to the arrangement of transcriptional complexes. J Cell Science 22:503–519Google Scholar
  33. Schmid M (1980) Chromosome banding in Amphibia. IV. Differentiation of GCand AT-rich chromosome regions in Anura. Chromosoma 77:83–103Google Scholar
  34. Schmid M, Olert J, Klett CH (1979) Chromosome banding in Amphibia. III. Sex chromosomes in Triturus. Chromosoma 71:29–55Google Scholar
  35. Schnedl W, Breitenbach M, Mikelsaar A-V, Stranzinger G (1977) Mithramycin and DIPI: a pair of fluorochromes specific for GC- and AT-rich DNA, respectively. Hum Genet 36:299–305Google Scholar
  36. Schweizer D (1976a) Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58:307–324Google Scholar
  37. Schweizer D (1976b) DAPI fluoresence of plant chromosomes prestained with actinomycin D. Exp Cell Res 102:408–413Google Scholar
  38. Sumner AT, Evans HJ (1973) Mechanisms involved in the banding of chromosomes with quinacrine and Giemsa. II. The interaction of the dyes with the chromosomal components. Exp Cell Res 81:223–236Google Scholar
  39. Varley JM, Macgregor HC, Nardi I, Andrews C, Erba HP (1980) Cytological evidence of transcription of highly repeated DNA sequences during the lampbrush stage in Triturus cristatus carnifex. Chromosoma 80:289–307Google Scholar
  40. Vlad M, Macgregor HC (1975) Chromomere number and its genetic significance in lampbrush chromosomes. Chromosoma 50:327–347Google Scholar
  41. Ward DC, Reich E, Goldberg I (1965) Base specificity in the interction of polynucleotides with antibiotic drugs. Science 149:1259–1263Google Scholar
  42. Zimmer C (1975) Effects of the antibiotics netropsin and distamycin A on the structure and function of nucleic acids. Progr Nucleic Acid Res Molec Biol 15:285–318Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • Simon H. Sims
    • 1
  • Herbert C. Macgregor
    • 1
  • Patricia S. Pellatt
    • 1
  • Heather A. Horner
    • 1
  1. 1.Department of ZoologyUniversity of LeicesterLeicesterEngland

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