Skip to main content
SpringerLink
Log in

Allocyclic behaviour and underreplication of the nucleolus chromosome in Pseudodiamesa (Chironomidae)

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The chironomid midge Pseudodiamesa branickii shows three polytene, banded elements in salivary gland and Malpighian tubule cells, none of which carry a nucleolar organizer. The present investigation revealed four chromosome pairs in mitotic metaphases, the nucleolus was localized in the tiny chromosome 4. Microphotometric determinations of the DNA contents in mitotic and salivary gland nuclei of Ps. branickii yielded a 2C value of 0.23 pg DNA and a maximum level of 12 endoreplications. In both salivary glands and Malpighian tubules, chromosome 4 appeared as a nonbanded network of chromatin in Feulgen preparations. Indirect immunofluorescent staining with antibodies specific for RNA·DNA hybrids indicated that this structure was transcriptionally active. Its reaction to heavy metal staining suggested that it included the nucleolar organizer, and this was conclusively demonstrated by in situ hybridization with 125I-rRNA. Chromosome pair 4 comprises about 11.4% of the total DNA in metaphase, but only 3.7% in the highly polytene salivary gland complement. According to a numerical simulation, the degree of underrepresentation suggests that about 70% of chromosome 4 is precluded from polytenization. The allocyclic aspect is probably due to this underreplication, with the nucleolar activity causing a structural loosening of the rest of the chromosome. The possible nature of the underreplicated sequences is discussed in the light of recent work on molecular aspects of rDNA structure in various Diptera.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Beckingham K (1982) Insect rDNA. In: Busch H, Rothblum L (eds) The cell nucleus, vol 10. Academic Press, New York, pp205–269

    Google Scholar 

  • Beckingham K, Thompson N (1982) Under-replication of intron+ rDNA cistrons in polyploid nurse cell nuclei of Calliphora erythrocephala. Chromosoma 87:177–196

    Google Scholar 

  • Beermann W (1962) Riesenchromosomen. Protoplasmatologia 6 D. Springer, Wien, pp 135–141

    Google Scholar 

  • Brutlag D, Appels R, Dennis ES, Peacock WJ (1977) Highly repeated DNA in Drosophila melanogaster. J Mol Biol 112:31–47

    Google Scholar 

  • Büsen W, Amabis JM, Leoncini O, Stollar BD, Lara FJS (1982) Immunofluorescent characterization of DNA·RNA hybrids on polytene chromosomes of Trichosia pubescens (Diptera, Sciaridae). Chromosoma 87:247–262

    Google Scholar 

  • Degelmann A, Royer H-D, Hollenberg CP (1979) The organization of the ribosomal RNA genes of Chironomus tentans and some closely related species. Chromosoma 71:263–281

    Google Scholar 

  • Dennhöfer L (1982) Cytophotometric DNA determinations and autoradiographic studies in salivary gland nuclei from larvae with different karyotypes in Drosophila melanogaster. Chromosoma 86:123–147

    Google Scholar 

  • Dennhöfer L (1982) Underreplication during polytenization? Theor Appl Genet 63:193–199

    Google Scholar 

  • Endow SA, Glover DM (1979) Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17:597–605

    Google Scholar 

  • Fittkau EJ (1954) Chironomidenstudien. I. Pseudodiamesa belingi n sp. Beitr Entomol 4:84–98

    Google Scholar 

  • Franz G, Kunz W, Grimm Ch (1983) Determination of the region of rDNA involved in polytenization in salivary glands of Drosophila hydei. Mol Gen Genet 191:74–80

    Google Scholar 

  • Gall JG, Cohen EH, Polan ML (1971) Repetitive DNA sequences in Drosophila. Chromosoma 33:319–344

    Google Scholar 

  • Gambarini AG, Lara JS (1974) Underreplication of ribosomal cistrons in polytene chromosomes of Rhynchosciara. J Cell Biol 63:215–222

    Google Scholar 

  • Goetghebuer M (1939) Tendipedidae (Chironomidae), Subfamilie Diamesinae, die Imagines. In: Lindner E (ed) Die Fliegen der paläarktischen Region, vol 13d. Schweizerbart, Stuttgart, p 28

    Google Scholar 

  • Hennig W, Meer B (1971) Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nature New Biol 233:70–72

    Google Scholar 

  • Hollenberg CP (1976) Proportionate representation of rDNA and Balbiani ring DNA in polytene chromosomes of Chironomus tentans. Chromosoma 57:185–197

    Google Scholar 

  • Israelewski N, Schmidt ER (1982) Spacer size heterogeneity in ribosomal DNA of Chironomus thummi is due to a 120 bp repeat homologous to a predominantly centromeric repeated sequence. Nucleic Acids Res 10:7689–7700

    Google Scholar 

  • Keyl H-G (1960) Die cytologische Diagnostik der Chironomiden. II. Diagnosen der Geschwisterarten Chironomus acidophilus n sp und Ch uliginosus n sp. Arch Hydrobiol 57:187–195

    Google Scholar 

  • Keyl H-G (1961) Die cytologische Diagnostik der Chironomiden. III. Diagnose von Chironomus parathummi n sp und Ergänzungen zur Bestimmungstabelle. Arch Hydrobiol 58:1–6

    Google Scholar 

  • Keyl H-G, Keyl I (1959) Die cytologische Diagnostik der Chironomiden. I. Bestimmungstabelle für die Gattung Chironomus auf Grund der Speicheldrüsen-Chromosomen. Arch Hydrobiol 56:43–57

    Google Scholar 

  • Kieffer JJ (1924) Chironomides nouveaux ou rares de l'Europe centrale. Bull Soc Hist Nat Moselle 30:11–110

    Google Scholar 

  • Kitagawa Y, Stollar BD (1982) Comparison of poly(A)·poly (dT) and poly (I)·poly (dC) as immunogens for the induction of antibodies to RNA·DNA hybrids. Mol Immunol 19:413–420

    Google Scholar 

  • Kuberskaya EF (1974) On the characteristics of the karyotype and some special features of the nucleus structure in Pseudodiamesa nivosa from the Lake Baikal area. Russ. Tsitologiya 16:1426–1432

    Google Scholar 

  • Kuberskaya EF (1979) Kariotipicheskaya kharakteristika massovykh vidov podsemeistva Diamesinae (Diptera, Chironomidae) Pribaikalya. In: Chubareva LA (ed) Kariosistematika bespozvonochnykh zhivotnykh, Leningrad, pp 47–50

  • Kunz W, Grimm C, Franz G (1981a) Autonome Steuerung der rRNA Genzahl bei der Organdifferenzierung von Drosophila hydei: eine Abweichung von der Regel der Genomkonstanz. Verh Dtsch Zool Ges 74:127–133

    Google Scholar 

  • Kunz W, Petersen G, Renkawitz-Pohl R, Glätzer KH, Schäfer M (1981b) Distribution of spacer length classes and the intervening sequence among different nucleolus organizers in Drosophila hydei. Chromosoma 83:145–158

    Google Scholar 

  • Lakhotia SC (1984) Replication in Drosophila chromosomes. XII. Reconfirmation of underreplication of heterochromatin in polytene nuclei by cytofluorometry. Chromosoma 89:63–67

    Google Scholar 

  • Lamb MJ (1982) The DNA content of polytene nuclei in midgut and Malpighian tubule cells of adult Drosophila melanogaster. Wilh Roux's Arch 191:381–384

    Google Scholar 

  • Melland AM (1941) The salivary glands of Prodiamesa olivacea. A case of asymmetry in the Diptera. J Hered 32:165–167

    Google Scholar 

  • Murray DA (1972) A list of the Chironomidae (Diptera) known to occur in Ireland, with notes on their distribution. Proc R Ir Acad B 72:275–293

    Google Scholar 

  • Nowicki M (1873) Beiträge zur Kenntniss der Dipterenfauna Galiziens. Jagellonische Universitäts-Buchdruckerei, Krakau, pp 3–6

    Google Scholar 

  • Pagast F (1947) Systematik und Verbreitung der um die Gattung Diamesa gruppierten Chironomiden. Arch Hydrobiol 41:435–596

    Google Scholar 

  • Pedersen BV (1978) Studies on the taxonomy of Chironomus islandicus (Kieffer 1913) (Diptera: Chironomidae). Entomol Scand 9:309–311

    Google Scholar 

  • Pelling C, Beermann W (1966) Diversity and variation of the nucleolar organizing regions in chironomids. Natl Cancer Inst Monogr 23:393–409

    Google Scholar 

  • Poulson DF, Metz CW (1938) Studies on the structure of nucleolus forming regions and related structures in the giant salivary gland chromosomes of Diptera. J Morphol 63:363–395

    Google Scholar 

  • Rasch EM, Barr HJ, Rasch RW (1971) The DNA content of sperm of Drosophila melanogaster. Chromosoma 33:1–18

    Google Scholar 

  • Renkawitz R, Kunz W (1975) Independent replication of the ribosomal RNA genes in the polytrophic-meroistic ovaries of Calliphora erythrocephala, Drosophila hydei, and Sarcophaga barbata. Chromosoma 53:131–140

    Google Scholar 

  • Renkawitz-Pohl R, Glätzer KH, Kunz W (1981) Ribosomal RNA genes with an intervening sequence are clustered within the X chromosomal ribosomal DNA of Drosophila hydei. J Mol Biol 148:95–101

    Google Scholar 

  • Robert M (1971) Einfluß von Ionenstärke und pH auf die differentielle Dekondensation der Nukleoproteide isolierter Speichel-drüsen-Zellkerne und -Chromosomen von Chironomus thummi. Chromosoma 36:1–33

    Google Scholar 

  • Roberts PA (1979) Rapid change of chromomeric and pairing patterns of polytene chromosome tips in D. melanogaster: migration of polytene-nonpolytene transition zone? Genetics 92:861–878

    Google Scholar 

  • Rudkin GT (1965) The structure and function of heterochromatin. In: Geerts SJ (ed) Genetics today. Proc XI Int Congr Genet, vol 2, Pergamon Press, Oxford, pp 359–374

    Google Scholar 

  • Schmidt ER, Godwin EA (1983) The nucleotide sequence of an unusual non-transcribed spacer and its ancestor in the rDNA in Chironomus thummi. EMBO J 2:1177–1183

    Google Scholar 

  • Serra-Tosio B (1976) Chironomides des Alpes: le genre Pseudodiamesa (Diptera, Chironomidae). Trav Sci Park Nat Vanoise 7:117–138

    Google Scholar 

  • Sinibaldi RM, Cummings MR (1981) Localization and characterization of rDNA in Drosophila tumiditarsus. Chromosoma 81:655–671

    Google Scholar 

  • Sokoloff S, Zacharias H (1977) Functional significance of changes in the shape of the polytene X chromosome in Phryne. Chromosoma 63:359–384

    Google Scholar 

  • Stocken JC (1975) Uranyl-EDTA-Hematoxylin: a new selective staining technique for nucleolar material. Histochemistry 43:313–322

    Google Scholar 

  • Thienemann A (1954) Chironomus. Leben, Verbreitung und wirtschaftliche Bedeutung der Chironomiden. Schweizerbart, Stuttgart, p 834

    Google Scholar 

  • Thienemann A, Mayer K (1933) Chironomiden-Metamorphosen. VI. Die Metamorphosen zweier hochalpiner Chironomiden (Dipt). Zool Anz 103:1–12

    Google Scholar 

  • Vogt P, Hennig W (1983) Y chromosomal DNA of Drosophila hydei. J Mol Biol 167:37–56

    Google Scholar 

  • Wülker W (1959) Diamesarien-Studien (Dipt, Chironomidae) im Hochschwarzwald. Arch Hydrobiol Suppl 24, 3:338–360

    Google Scholar 

  • Zacharias H (1979) Underreplication of a polytene chromosome arm in the chironomid Prodiamesa olivacea. Chromosoma 72:23–51

    Google Scholar 

  • Zacharias H (1981) Sex-linked difference in DNA content of a polytene chromosome in Prodiamesa (Chironomidae). Chromosoma 82:657–672

    Google Scholar 

  • Zaha A, Leoncini O, Hollenberg CP, Lara FJS (1982) Cloning and characterization of the ribosomal RNA genes of Rhynchosciara americana. Chromosoma 87:103–116

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoologisches Institut der Universität, Biologiezentrum, Olshausenstraße 40-60, D-2300, Kiel, Federal Republic of Germany

    Helmut Zacharias

Authors
  1. Helmut Zacharias
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zacharias, H. Allocyclic behaviour and underreplication of the nucleolus chromosome in Pseudodiamesa (Chironomidae). Chromosoma 89, 263–273 (1984). https://doi.org/10.1007/BF00292473

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00292473

Keywords

Search

Navigation