Skip to main content
Log in

Individual variations in the content of giant secretory polypeptides in salivary glands of Chironomus

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Salivary glands in aquatic larvae of Chironomus are responsible for formation of a fiber that larvae use to construct feeding tubes. Major constituents of this fiber include a family (the sp-I family) of high M r (1 × 106) secretory polypeptides. Because of our interest in the polypeptide composition and polymerization of the salivary fiber we conducted a survey of the electrophoretic pattern of sp-I components found in salivary glands obtained from individual larvae. The survey encompassed ten strains of Chironomus tentans, three strains of Chironomus pallidivittatus and four strains of Chironomus thummi. Salivary glands from C. tentans and C. pallidivittatus contained at least four sp-I components (sp-Ia, sp-Ib, sp-Ic and sp-Id) that behave identically with regard to their electrophoretic mobility and detectability when larvae were exposed to galactose or glycerol. Sp-I components in C. thummi were generally fewer and not directly comparable by electrophoretic mobility to sp-I components in the other two species. During this survey two important alterations were observed in the electrophoretic pattern of sp-I components obtained from C. tentans and C. pallidivittatus. First, all four sp-I components exhibited, with a low frequency, double bands that appeared as slow-versus-fast electrophoretic variants of a particular component. Secondly, the relative steady-state level of each sp-I component fluctuated in comparison to other sp-I components in the same extract. This fluctuation varied such that any one sp-I component might appear as a single prominent component. Sp-I components are encoded by a multigene family located in Balbiani rings (BRs). Results presented here, in conjunction with known nucleotide sequence data from BR genes, led us to the following conclusions. The slow and fast electrophoretic variants observed for each sp-I component suggest that each corresponding BR gene may be able to expand and/or contract in size. The observed degree of independent fluctuation in the steady-state level of each sp-I component suggests that each BR gene may be able to regulate its expression independently from the others. Finally, the observation that salivary glands sometimes contained only one prominent sp-I component led us to hypothesize that, whereas salivary fibers might typically be heteropolymers comprised of two or more types of sp-I components, homopolymers comprised of only one sp-I component may also exist.

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

  • Beermann W (1973) Directed changes in the pattern of Balbiani ring puffing in Chironomus. Chromosoma 41:297–326

    Google Scholar 

  • Case ST (1986) Correlated changes in the steady-state levels of Balbiani ring mRNAs and secretory polypeptides in salivary glands of Chironomus tentans. Chromosoma 94:483–491

    Google Scholar 

  • Case ST, Daneholt B (1977) Cellular and molecular aspects of genetic expression in Chironomus salivary glands. In: Paul J (ed) International review of biochemistry, vol. 15. University Park Press, Baltimore, pp 45–77

    Google Scholar 

  • Darby RE (1962) Midges associated-with California rice fields, with special reference to their ecology (Diptera: Chironomidae). Hilgardia 32:1–206

    Google Scholar 

  • Edström J-E, Rydlander L, Francke C (1980) Concomitant induction of a Balbiani ring and a giant secretory protein in Chironomus salivary glands. Chromosoma 81:115–124

    Google Scholar 

  • Edström J-E, Sierakowska H, Burval K (1982) Dependence of Balbiani ring induction in Chironomus salivary glands on inorganic phosphate. Dev Biol 91:131–137

    Google Scholar 

  • Galler R, Rydlander L, Riedel N, Kluding H, Edström J-E (1984) Balbiani ring induction in phosphate metabolism. Proc Natl Acad Sci USA 81:1448–1452

    Google Scholar 

  • Galler R, Saiga H, Widmer RM, Lezzi M, Edström J-E (1985) Two genes in Balbiani ring 2 with metabolically different 75S transcripts. EMBO J. 4:2977–2982

    Google Scholar 

  • Grossbach U (1969) Chromosomen-Aktivität und biochemische Zelldifferenzierung in den Speicheldrüsen von Camptochironomus. Chromosoma 28:136–187

    Google Scholar 

  • Grossbach U (1977) The salivary gland of Chironomus (Diptera): a model system. In: Beermann W (ed) Results and problems in cell differentiation, vol. 8. Springer, Berlin Heidelberg New York, pp 147–196

    Google Scholar 

  • Hamodrakas SJ, Kafatos FC (1984) Structural implications of primary sequences from a family of Balbiani ring-encoded proteins in Chironomus. J Mol Evol 20:296–303

    Google Scholar 

  • Hertner T, Meyer B, Eppenberger HM, Mähr R (1980) The secretion proteins of Chironomus tentans salivary glands: electrophoretic characterization and molecular weight estimation. Roux's Arch Dev Biol 189:69–72

    Google Scholar 

  • Hertner T, Eppenberger HM, Lezzi M (1983) The giant secretory proteins of Chironomus tentans salivary glands: the organization of their primary structure, their amino acid and carbohydrate composition. Chromosoma 88:194–200

    Google Scholar 

  • Hodkinson ID, Williams KA (1980) Tube formation and distribution of Chironomus plumosus L. (Diptera: Chironomidae) in a eutrophic woodland pond. In: Murray D (ed) Chironomidae: ecology, systematics, cytology and physiology, Pergamon, Oxford, pp 331–337

    Google Scholar 

  • Kao W-Y, Case ST (1985) A novel giant secretion polypeptide in Chironomus salivary glands: implications for another Balbiani ring gene. J Cell Biol 101:1044–1051

    Google Scholar 

  • Mähr R, Meyer B, Daneholt B, Eppenberger HM (1980) Activation of Balbiani ring genes in Chironomus tentans after a pilocarpine-induced depletion of the secretory products from the salivary gland lumen. Dev Biol 80:409–418

    Google Scholar 

  • McLachlan AJ (1977) Some effects of tube shape on the feeding of Chironomus plumosus L. (Diptera: Chironomidae). J Anim Ecol 46:139–146

    Google Scholar 

  • McLachlan AJ, Cantrell MA (1976) Sediment development and its influence on the distribution and tube structure of Chironomus plumosus L. (Chironomidae, Diptera) in a new impoundment. Freshwater Biol 6:437–443

    Google Scholar 

  • Muskavitch MAT, Hogness DS (1982) An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell 29:1041–1051

    Google Scholar 

  • Nelson L, Daneholt B (1981) Modulation of RNA synthesis in the Balbiani rings of Chironomus tentans with galactose treatment. Chromosoma 83:645–659

    Google Scholar 

  • Oliver DR (1971) Life history of the Chironomidae. Ann Rev Entomol 16:211–230

    Google Scholar 

  • Pustell J, Kafatos FC, Wobus U, Bäumlein H (1984) Balbiani ring DNA: sequence comparisons and evolutionary history of a family of hierarchically repetitive protein-coding genes. J Mol Evol 20:281–295

    Google Scholar 

  • Rydlander L (1984) Isolation and characterization of the two giant secretory proteins in salivary glands of Chironomus tentans. Biochem J 220:423–431

    Google Scholar 

  • Rydlander L, Edström J-E (1980) Large size nascent protein as dominating component during protein synthesis in Chironomus salivary glands. Chromosoma 81:85–99

    Google Scholar 

  • Sass H (1982) RNA polymerase B in polytene chromosomes: immunofluorescent and autoradiographic analysis during stimulated and repressed RNA synthesis. Cell 28:269–278

    Google Scholar 

  • Scott KMF (1967) The larval and pupal stages of the midge Tanytarsus (Rheotanytarsus) fuscus Freeman (Diptera: Chironomidae). J Entomol Soc S Afr 30:174–184

    Google Scholar 

  • Serfling E, Meyer L, Rudolph A, Stiner K (1983) Secretory proteins and Balbiani ring gene activities in salivary glands of Chironomus thummi larvae. Chromosoma 88:16–23

    Google Scholar 

  • Sprague KU, Roth MB, Manning RF, Gage LP (1979) Alleles of the fibroin gene coding for proteins of different lengths. Cell 17:407–413

    Google Scholar 

  • Walentowicz AT, McLachlan AJ (1980) Chironomids and particles: a field experiment with peat in an upland stream. In: Murray D (ed) Chironomidae: ecology, systematics, cytology and physiology, Pergamon, Oxford, pp 179–185

    Google Scholar 

  • Wallace JB, Merritt RW (1980) Filter-feeding ecology of aquatic insects. Ann Rev Entomol 25:103–132

    Google Scholar 

  • Walshe BM (1951) The feeding habits of certain Chironomid larvae (subfamily tendipedinae). Proc Zool Soc London 121:63–79

    Google Scholar 

  • Wieslander L, Höög C, Höög J-O, Jörnvall H, Lendahl U, Daneholt B (1984) Conserved and nonconserved structures in the secretory proteins encoded in the Balbiani ring genes of Chironomus tentans. J Mol Evol 20:304–312

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kao, WY., Case, S.T. Individual variations in the content of giant secretory polypeptides in salivary glands of Chironomus . Chromosoma 94, 475–482 (1986). https://doi.org/10.1007/BF00292757

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00292757

Keywords

Navigation