Skip to main content
SpringerLink
Log in

The lysozyme locus in Drosophila melanogaster: different genes are expressed in midgut and salivary glands

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

As part of a study of the genes involved in antibacterial defense in Drosophila melanogaster, we have isolated genomic clones harboring a family of chicken-type lysozyme genes, using a lepidopteran lysozyme cDNA as probe. The locus was mapped to the cytological location 61F1-4 on the third chromosome and two of the genes at this locus, LysD and LysP, were analyzed in detail. In contrast to the bacteria-induced lysozymes in the hemolymph of many insects, the transcription levels of both Drosophila genes decrease after bacterial injections into the hemocoel. Apparently, these gene products, like the specifically adapted lysozymes in mammalian foregut fermenters, have been recruited for the digestion of bacteria present in fermenting food. The LysD gene is expressed in an anterior section of the midgut during all feeding stages of development in both larvae and adults. The LysP gene is only active in the adult where it is expressed in the salivary glands. The transcription units for both genes are very compact and they lack introns. Lysozyme D is unusual in that it is predicted to have an acidic isoelectric point whereas lysozyme P appears to be a typical basic lysozyme.

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

  • Akam M (1983) The location of Ultrabithorax transcripts in Drosophila tissue sections. EMBO J 2:2075–2084

    Google Scholar 

  • Akam M, Martínez-Arias A (1985) The distribution of Ultrabithorax transcripts in Drosophila embryos. EMBO J 4:1689–1700

    Google Scholar 

  • Begon M (1982) Yeasts and Drosophila. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila, vol 3b. Academic Press, London, pp 345–384

    Google Scholar 

  • Bodenstein D (1950) The postembryonic development of Drosophila. In: Demerec M (ed) Biology of Drosophila. John Wiley and Sons, New York, pp 275–367

    Google Scholar 

  • Boman HG, Hultmark D (1987) Cell-free immunity in insects. Annu Rev Microbiol 41:103–126

    Google Scholar 

  • Boman HG, Nilsson I, Rasmuson B (1972) Inducible antibacterial defence system in Drosophila. Nature 237:232–235

    Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Google Scholar 

  • Browne WJ, North ACT, Phillips DC, Brew K, Vanaman TC, Hill RL (1969) A possible three-dimensional structure of bovine α-lactalbumin based on that of hen's egg-white lysozyme. J Mol Biol 42:65–86

    Google Scholar 

  • Chung LP, Keshav S, Gordon S (1988) Cloning the human lysozyme cDNA: inverted Alu repeat in the mRNA and in situ hybridization for macrophages and Paneth cells. Proc Natl Acad Sci USA 85:6227–6231

    Google Scholar 

  • Davis CA, Riddell DC, Higgins MJ, Holden JJ, White BN (1985) A gene family in Drosophila melanogaster coding for trypsin-like enzymes. Nucleic Acids Res 13:6605–6619

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Doane WW, Thompson DB, Norman RA, Hawley SA (1990) Molecular genetics of a three-gene cluster in the Amy region of Drosophila. Prog Clin Biol Res 344:19–48

    Google Scholar 

  • Dobson DE, Prager EM, Wilson AC (1984) Stomach lysozymes of ruminants. I. Distribution and catalytic properties. J Biol Chem 259:11607–11616

    Google Scholar 

  • Engström Å, Xanthopoulos KG, Boman HG, Bennich H (1985) Amino acid and cDNA sequences of lysozyme from Hyalophora cecropia. EMBO J 4:2119–2122

    Google Scholar 

  • Espinoza-Fuentes FP, Terra WR (1987) Physiological adaptations for digesting bacteria. Water fluxes and distribution of digestive enzymes in Musca domestica larval midgut. Insect Biochem 17:809–817

    Google Scholar 

  • Filshie BK, Poulson DF, Waterhouse DF (1971) Ultrastructure of the copper-accumulating region of the Drosophila midgut. Tissue Cell 3:77–102

    Google Scholar 

  • Flyg C, Dalhammar G, Rasmuson B, Boman HG (1987) Insect immunity. Inducible antibacterial activity in Drosophila. Insect Biochem 17:153–160

    Google Scholar 

  • Gilman M (1987) Ribonuclease protection assay. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. John Wiley and Sons, New York, pp 4.7.1–4.7.8

    Google Scholar 

  • Go M (1983) Modular structural units, exons, and function in chicken lysozyme. Proc Natl Acad Sci USA 80:1964–1968

    Google Scholar 

  • Hafen E, Levine M (1986) The localization of RNAs in Drosophila sections by in situ hybridization. In: Roberts DB (ed) Drosophila: a practical approach. IRL Press, Oxford, pp 139–157

    Google Scholar 

  • Hafen E, Levine M, Garber RL, Gehring WJ (1983) An improved in situ hybridization method for the detection of cellular RNAs in Drosophila tissue sections and its application for localizing transcripts of the homeotic Antennapedia gene complex. EMBO J 2:617–623

    Google Scholar 

  • Henikoff S, Wallace JC (1988) Detection of protein similarities using nucleotide sequence databases. Nucleic Acids Res 16:6191–6204

    Google Scholar 

  • Hultmark D, Klemenz R, Gehring WJ (1986) Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell 44:429–438

    Google Scholar 

  • Jollès P, Jollès J (1984) What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem 63:165–189

    Google Scholar 

  • Kaiser K, Murray NE (1985) The use of phage lambda replacement vectors in the construction of representative genomic libraries. In: Glover DM (ed) DNA cloning: a practical approach, vol 1. IRL Press, Oxford, pp 1–47

    Google Scholar 

  • Kylsten P, Samakovlis C, Hultmark D (1990) The cecropin locus in Drosophila; a compact gene cluster involved in the response to infection. EMBO J 9:217–224

    Google Scholar 

  • Lefevre G Jr (1976) A photographic representation and interpretation of the polytene chromosomes of Drosophila melanogaster salivary glands. In: Ashburner M, Novitski E (eds) The genetics and biology of Drosophila, vol 1a. Academic Press, London, pp 31–66

    Google Scholar 

  • Maniatis T, Hardison RC, Lacy E, Lauer J, O'Connell C, Quon D, Sim GK, Efstratiadis A (1978) The isolation of structural genes from libraries of eukaryotic DNA. Cell 15:687–701

    Google Scholar 

  • Martin M, Mettling C, Giangrande A, Ruiz C, Richards G (1989) Regulatory elements and interactions in the Drosophila 68C glue gene cluster. Dev Genet 10:189–197

    Google Scholar 

  • McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ (1984) A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308:428–433

    Google Scholar 

  • Miller A (1950) The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. John Wiley and Sons, New York, pp 420–534

    Google Scholar 

  • Mohrig W, Messner B (1968a) Immunreaktionen bei Insekten I. Lysozym als grundlegender antimikrobieller Faktor im humoralen Abwehrmechanismus der Insekten. Biol Zentralbl 87:439–470

    Google Scholar 

  • Mohrig W, Messner B (1968b) Immunreaktionen bei Insekten II. Lysozym als antimikrobielles Agens im Darmtrakt von Insekten. Biol Zentralbl 87:705–718

    Google Scholar 

  • Pardue ML (1986) In situ hybridization to DNA of chromosomes and nuclei. In: Roberts DB (ed) Drosophila: a practical approach. IRL Press, Oxford, pp 111–137

    Google Scholar 

  • Proudfoot NJ, Brownlee GG (1976) 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214

    Google Scholar 

  • Robertson M, Postlethwait JH (1986) The Immoral antibacterial response of Drosophila adults. Dev Comp Immunol 10:167–179

    Google Scholar 

  • Samakovlis C, Kimbrell DA, Kylsten P, Engström Å, Hultmark D (1990) The immune response in Drosophila: pattern of cecropin expression and biological activity. EMBO J 9:2969–2976

    Google Scholar 

  • Samakovlis C, Kylsten P, Kimbrell DA, Engström Å, Hultmark D (1991) The Andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. EMBO J 10:163–169

    Google Scholar 

  • Snyder M, Davidson N (1983) Two gene families clustered in a small region of the Drosophila genome. J Mol Biol 166:101–118

    Google Scholar 

  • Stewart CB, Schilling JW, Wilson AC (1987) Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404

    Google Scholar 

  • Strasburger M (1932) Ban, Funktion, und Variabilität des Darmtraktes von Drosophila melanogaster Meigen. Z wiss Zool 140:539–649

    Google Scholar 

  • Sun S-C, Åsling B, Faye I (1991) Organization and expression of the immunoresponsive lysozyme gene in the giant silk moth, Hyalophora cecropia. J Biol Chem 266:6644–6649

    Google Scholar 

  • Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200

    Google Scholar 

  • Wicker C, Reichhart J-M, Hoffmann D, Hultmark D, Samakovlis C, Hoffmann JA (1990) Insect immunity. Characterization of a Drosophila cDNA encoding a novel member of the diptericin family of immune peptides. J Biol Chem 265:22493–22498

    Google Scholar 

  • Yun Y, Davis RL (1989) Levels of RNA from a family of putative serine protease genes are reduced in Drosophila melanogaster dunce mutants and are regulated by cyclic AMP. Mol Cell Biol 9:692–700

    Google Scholar 

Download references

Author information

Author notes

  1. Per Kylsten

    Present address: Department of Biochemistry, Adelaide University, G.P.O. Box 498, 5001, Adelaide, South Australia, Australia

  2. Deborah A. Kimbrell

    Present address: Department of Biology, University of Houston, 77204-5513, Houston, Texas, USA

  3. Christos Samakovlis

    Present address: Department of Biochemistry, School of Medicine, Stanford University Medical Center, 94305-5307, Stanford, California, USA

Authors and Affiliations

  1. Department of Molecular Biology, Stockholm University, S-106 91, Stockholm, Sweden

    Per Kylsten, Deborah A. Kimbrell, Sirlei Daffre, Christos Samakovlis & Dan Hultmark

Authors
  1. Per Kylsten
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deborah A. Kimbrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sirlei Daffre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christos Samakovlis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dan Hultmark
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by M. Ashburner

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kylsten, P., Kimbrell, D.A., Daffre, S. et al. The lysozyme locus in Drosophila melanogaster: different genes are expressed in midgut and salivary glands. Molec. Gen. Genet. 232, 335–343 (1992). https://doi.org/10.1007/BF00266235

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00266235

Key words

Search

Navigation