Skip to main content
SpringerLink
Log in

The sequence and expression pattern of the Calliphora erythrocephala yolk protein A and B genes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The yolk protein genes (yps) are expressed in a temporal, tissue- and sex-specific fashion in Drosophila melanogaster. Here we report the sequence of two related genes in Calliphora erythrocephala. The predicted Calliphora yolk protein (YP) sequences are well conserved, especially at the C-terminal end when compared to those of D. melanogaster and Ceratitis capitata. Database searches with the Calliphora yolk protein B (CeYPB) sequence identify the vertebrate lipase similarity reported for the YPs of Drosophila and Ceratitis. Moreover, sequences with identity to divalent ion-binding sites were observed, which colocalized with putative tyrosine sulfation sites. Calliphora oogenesis differs from Drosophila in that it is cyclic in response to a meat feed. The Calliphora yp genes are expressed in the follicle cells of the egg chamber during vitellogenesis, as shown by in situ hybridization, and the yp message levels correlate with YP synthesis. The synthesis of the yp transcripts in ovaries of Calliphora occurs in the same pattern as that for ovarian transcripts in Drosophila. In the carcass, yp transcript levels are correlated with the production of a batch of eggs.

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

  • Abrahamsen N, Martinez A, Kjaer T, Sondergaard L, Bownes M (1993) Cis-regulatory sequences leading to the fat body, sex specific, expression of the yolk protein genes 1 and 2 of Drosophila melanogaster. Mol Gen Genet 237:41–48

    Google Scholar 

  • Adams TS, Hagedorn HH, Wheelock GH (1985) Haemolymph ecdysteroid in the housefly, Musca domestica, during oogenesis and its relationship with vitellogenin levels. J Insect Physiol 31:91–97

    Google Scholar 

  • Baeuerle PA, Huttner WB (1985) Tyrosine sulfation of yolk proteins 1, 2 and 3 in Drosophila melanogaster. J Biol Chem 260:6434–6439

    Google Scholar 

  • Beverley MS, Wilson AC (1982) Molecular evolution in Drosophila and the higher Diptera I. Micro-complement fixation studies of a larval haemolymph protein. J Mol Evol 18:251–264

    Google Scholar 

  • Beverley MS, Wilson AC (1984) Molecular evolution in Drosophila and the higher Diptera 11. A time scale for fly evolution. J Mol Evol 21:1–13

    Google Scholar 

  • Bownes M (1980) The use of yolk protein variations in Drosophila species to analyse the control of vitellogenesis. Differentiation 16:109–116

    Google Scholar 

  • Bownes M (1990) The yolk proteins and their genes in Drosophila. Prog Comp Endocrin 342:336–342

    Google Scholar 

  • Bownes M, Nöthiger R (1981) Sex determining genes and vitellogenin synthesis in Drosophila melanogaster. Mol Gen Genet 182:222–228

    Google Scholar 

  • Bownes M, Blair M, Kozma R, Dempster M (1983) 20-hydroxyecdysone stimulates tissue-specific yolk-protein gene transcription in both male and female Drosophila. J Embryol Exp Morphol 78:249–268

    Google Scholar 

  • Bownes M, Blair M (1986) The effect of a sugar diet and hormones on the expression of the Drosophila yolk protein genes. J Insect Physiol 32:493–501

    Google Scholar 

  • Bownes M, Scott A, Shirras A (1988a) Dietary components modulate yolk protein gene transcription in Drosophila melanogaster. Development 103:119–128

    Google Scholar 

  • Bownes M, Shirras A, Blair M, Collins J, Coulson A (1988b) Evidence that insect embryogenesis is regulated by ecdysteroids released from yolk proteins. PNAS USA 85:1554–1557

    Google Scholar 

  • Brennan MD, Warren TG, Mahowald AP (1980) Signal peptides and signal peptidases in Drosophila melanogaster. J Cell Biol 87:516–520

    Google Scholar 

  • Brennan MD, Weiner AJ, Goralski TJ, Mahowald AP (1982) The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev Biol 89:225–236

    Google Scholar 

  • Burtis KC, Coschigano KT, Baker BS, Wensink PC (1991) Drosophila doublesex protein binds to a sex-specific yolk protein gene enhancer. EMBO J 10:2577–2582

    Google Scholar 

  • Cherbas L, Schulz RA, Koehler MMD, Savakis C, Cherbas P (1986) Structure of the Eip28/29 gene, an ecdysone-inducible gene from Drosophila. J Mol Biol 189:617–631

    Google Scholar 

  • DiMario PJ, Mahowald AP (1986) The effect of pH and weak bases on the in vitro endocytosis of vitellogenin by oocytes of Drosophila melanogaster. Cell Tissue Res 246:103–108

    Google Scholar 

  • DiMario PJ, Warren TG, Mahowald AP (1987) The purification and in vitro phosphorylation of vitellogenin from Drosophila melanogaster. Insect Biochem 17:1187–1197

    Google Scholar 

  • Fenerjian MG, Martinez-Cruzado JC, Swimmer C, King D, Kafatos FC (1989) Evolution of the autosomal chorion cluster in Drosophila II. Chorion gene expression and sequence comparisons of hte s16 and s19 genes in evolutionarily distant species. J Mol Evol 29:108–125

    Google Scholar 

  • Fraenkel G (1940) Utilisation and digestion of carbohydrates by adult blowfly. J Exp Biol 17:18–29

    Google Scholar 

  • Garabedian MJ, Shepherd BM, Wensink PC (1986) A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell 45:859–867

    Google Scholar 

  • Garabedian MJ, Shirras AD, Bownes M, Wensink PC (1987) The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene 55:1–8

    Google Scholar 

  • Geysen J, Cardeon J, De Loof A (1986) Distribution of yolk polypeptides in the follicle cells during differentiation of the follicular epithelium in Sarcophaga bullata egg follicles. Development 101:33–44

    Google Scholar 

  • Gochoco CH, Kunkel JG, Nordin JH (1988) Experimental modification of an insect vitellin affects its structure and its uptake by oocytes. Arch Insect Biochem Physiol 9:179–199

    Google Scholar 

  • Goodman T, Morrison PE, Davies DM (1968) Cytological changes with developing ovary of the house fly fed milk and other diets. Can J Zool 46:409–421

    Google Scholar 

  • Guild G, Richards G (1992) Ecdysone and the onion. Nature 357:539

    Google Scholar 

  • Hatzopoulos P, Kambysellis MP (1987) Isolation and structural analysis of the vitellogenin genes from Drosophila grimshawi. Mol Gen Genet 206:475–484

    Google Scholar 

  • Hortin GL, Folz R, Gordon RI, Strauss AW (1986) Characterisation of sites of tyrosine sulfation in proteins and criteria for predicting their occurrence. Biochem Biophys Res Comm 141:326–333

    Google Scholar 

  • Hung M, Barnett T, Woolford C, Wensink PC (1982) Transcript maps of Drosophila yolk protein genes. J Mol Biol 154:581–602

    Google Scholar 

  • Hung M, Wensink PC (1983) Sequence and structure conservation in yolk proteins and their genes. J Mol Biol 164:481–489

    Google Scholar 

  • Huttner WB, Baeuerle PA (1988) Protein sulfation on tyrosine. Modern Cell Biol 6:97–140

    Google Scholar 

  • Huybrechts R, De Loof A (1982) Similarities in vitellogenin and control of vitellogenin synthesis within the genera Sarcophaga, Calliphora, Phormia and Lucilia (Diptera). Comp Biochem Physiol 72B:339–344

    Google Scholar 

  • Jeffery J, Perssons B, Jornvall H (1987) Characteristics of alcohol/polyol dehydrogenases. Eur J Biochem 167:195–201

    Google Scholar 

  • Kassis JA, Desplan C, Wright DK, O Farrell PH (1989) Evolutionary conservation of homeodomain-binding sites and other sequences upstream and within the major transcription unit of the Drosophila segmentation gene engrailed. Mol Cell Biol 9:4304–4311

    Google Scholar 

  • King RC (1970) Ovarian development of Drosophila melanogaster. Academic Press, New York

    Google Scholar 

  • Konsolaki M, Komitopoulou K, Tolias PP, King DL, Swimmer C, Kafatos FC (1990) The chorion genes of the medfly, Ceratitis capitata. I. structural and regulatory conservation of the s36 gene relative to two Drosophila species. Nucleic Acids Res 18:1731–1737

    Google Scholar 

  • Kozma R, Bownes M (1986a) Yolk protein induction in males of several Drosophila species. Insect Biochem 16:263–271

    Google Scholar 

  • Kozma R, Bownes M (1986b) Identification and comparison of the yolk polypeptides and the genes which code for them in D. melanogaster sibling species. Mol Gen Genet 204:302–309

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Lagueux M, Harry P, Hoffmann JA (1981) Ecdysteroids are bound to vitellin in newly laid eggs of Locusta. Mol Cell Endocrinol 24:325–338

    Google Scholar 

  • Liddell S, Bownes M (1991) Characterisation, molecular cloning and sequencing of yp3s1, a female yolk protein mutant in Drosophila. Mol Gen Genet 228:81–88

    Google Scholar 

  • Logan S, Garabedian MJ, Wensink PC (1989) DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev 3:1453–1461

    Google Scholar 

  • Logan S, Wensink PC (1990) Ovarian follicle cell enhancers from the Drosophila yolk protein genes: different segments of one enhancer have different cell-type specificities that interact to give normal expression. Genes Dev 4:613–623

    Google Scholar 

  • Martinez A, Bownes M (1992) The specificity of yolk protein uptake in Cyclorrhaphan Diptera is conserved through evolution. J Mol Evol 35:444–453

    Google Scholar 

  • Martinez-Cruzado JC, Swimmer C, Fenerejian MG, Kafatos FC (1988) Evolution of the autosomal chorion locus in Drosophila. 1. General organisation of the locus and sequence comparison of the genes s15 and s19 in evolutionarily distant species. Genetics 119:663–667

    Google Scholar 

  • Minoo P, Postlethwait J (1985) Biosynthesis of Drosophila yolk polypeptides. Arch Insect Biochem Physiol 2:7–27

    Google Scholar 

  • Osir EO, Anderson DR, Grimes WJ, Law JH (1986) Studies on the carbohydrate moiety of vitellogenin from the tobacco hornworm, Manduca sexta. Insect Biochem 16:471–478

    Google Scholar 

  • Perlman D, Halvorsen HO (1983) A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol 167:391–409

    Google Scholar 

  • Perssons B, Bertsson-Olovecrona G, Enerback S, Olivecrona T, Jornvall H (1989) Structural features of lipoprotein lipase. Eur J Biochem 179:39–45

    Google Scholar 

  • Postlethwait JH, Jowett T (1980) Genetic analysis of the hormonally regulated yolk polypeptide genes in D. melanogaster. Cell 20:671–678

    Google Scholar 

  • Postlethwait JH, Bownes M, Jowett T (1980) Sexual phenotype and vitellogenin synthesis in Drosophila melanogaster. Am Zool 21:687–700

    Google Scholar 

  • Riddihough G, Pelham HRB (1987) An ecdysone response element in the Drosophila hsp27 promotor. EMBO J 6:3729–3734

    Google Scholar 

  • Rina M, Mintzas AC (1988) Biosynthesis and regulation of two vitellogenins in the fat body and ovaries of Ceratitis capitata (Diptera). Roux's Arch Dev Biol 197:167–174

    Google Scholar 

  • Rina M, Savakis C (1991) A cluster of vitellogenin genes in the Mediterranean fruit fly Ceratitis capitata: sequence and structural conservation in Diptera yolk proteins and their genes. Genetics 127:769–780

    Google Scholar 

  • Rohrkasten A, Ferenz H-J (1986) Properties of the vitellogenin receptor of isolated locust oocyte membranes. Int J Inv Rep Dev 10:133–142

    Google Scholar 

  • Rubacha A, Tucker MA, De Valoir T, Berlikoff EJ, Bekingham K (1988) Genes with specific functions in the ovarian follicles of Calliphora erythrocephala (Diptera). Dev Biol 129:449–463

    Google Scholar 

  • Ruoslahti E, Pierschbacher MD (1986) Arg-Gly-Asp; a versatile cell recognition signal. Cell 44:517–518

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-termination inhibitors. PNAS USA 74:5463–5467

    Google Scholar 

  • Spieth J, Nettleton M, Zucker-Aprison E, Lea K, Blumenthal T (1991) Vitellogenin motifs conserved in nematodes and vertebrates. J Mol Evol 32:429–438

    Google Scholar 

  • Swimmer C, Fenerjian MG, Martinez-Cruzado JC, Kafatos FC (1990) Evolution of the autosomal chorion cluster in Drosophila III. Comparison of the s18 gene in evolutionarily distant species and interspecific control of chorion gene amplification. J Mol Biol 215:225–235

    Google Scholar 

  • Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridisation method for the localisation of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene Hunchback. Chromosoma 98:81–85

    Google Scholar 

  • Thomas PS (1980) Hybridisation of denatured RNA and small DNA fragments transferred to nitrocellulose. PNAS USA 77:5201–5205

    Google Scholar 

  • Treier M, Pfeifle C, Tautz D (1989) Comparison of the gap segmentation gene Hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J 8:1517–1525

    Google Scholar 

  • von Heijne G (1983) Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133:17–21

    Google Scholar 

  • Yan Y-L, Kunert C, Postlethwait JH (1987) Sequence homology among the three yolk polypeptide (Yp) genes in Drosophila melanogaster. Nucleic Acids Res 15:67–85

    Google Scholar 

Download references

Author information

Author notes

  1. Alberto Martinez

    Present address: Zentrum fur Molekulare Neurobiologie, Martinist. 52, Pav 42., 2000, Hamburg 20, Germany

Authors and Affiliations

  1. Institute of Cell and Molecular Biology, Darwin Building, Mayfield Road, EH9 3JR, Edinburgh, Scotland

    Alberto Martinez & Mary Bownes

Authors
  1. Alberto Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mary Bownes
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: M. Bownes

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martinez, A., Bownes, M. The sequence and expression pattern of the Calliphora erythrocephala yolk protein A and B genes. J Mol Evol 38, 336–351 (1994). https://doi.org/10.1007/BF00163151

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00163151

Key words

Search

Navigation