Skip to main content
Genetics logoLink to Genetics
. 1991 Apr;127(4):769–780. doi: 10.1093/genetics/127.4.769

A Cluster of Vitellogenin Genes in the Mediterranean Fruit Fly Ceratitis Capitata: Sequence and Structural Conservation in Dipteran Yolk Proteins and Their Genes

M Rina 1, C Savakis 1
PMCID: PMC1204404  PMID: 1903120

Abstract

Four genes encoding the major egg yolk polypeptides of the Mediterranean fruit fly Ceratitis capitata, vitellogenins 1 and 2 (VG1 and VG2), were cloned, characterized and partially sequenced. The genes are located on the same region of chromosome 5 and are organized in pairs, each encoding the two polypeptides on opposite DNA strands. Restriction and nucleotide sequence analysis indicate that the gene pairs have arisen from an ancestral pair by a relatively recent duplication event. The transcribed part is very similar to that of the Drosophila melanogaster yolk protein genes Yp1, Yp2 and Yp3. The Vg1 genes have two introns at the same positions as those in D. melanogaster Yp3; the Vg2 genes have only one of the introns, as do D. melanogaster Yp1 and Yp2. Comparison of the five polypeptide sequences shows extensive homology, with 27% of the residues being invariable. The sequence similarity of the processed proteins extends in two regions separated by a nonconserved region of varying size. Secondary structure predictions suggest a highly conserved secondary structure pattern in the two regions, which probably correspond to structural and functional domains. The carboxy-end domain of the C. capitata proteins shows the same sequence similarities with triacylglycerol lipases that have been reported previously for the D. melanogaster yolk proteins. Analysis of codon usage shows significant differences between D. melanogaster and C. capitata vitellogenins with the latter exhibiting a less biased representation of synonymous codons.

Full Text

The Full Text of this article is available as a PDF (3.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  2. Blobel G., Dobberstein B. Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J Cell Biol. 1975 Dec;67(3):852–862. doi: 10.1083/jcb.67.3.852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bodmer M., Ashburner M. Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species of Drosophila. 1984 May 31-Jun 6Nature. 309(5967):425–430. doi: 10.1038/309425a0. [DOI] [PubMed] [Google Scholar]
  4. Bownes M., Hames B. D. Analysis of the yolk proteins in Drosophila melanogaster. Translation in a cell free system and peptide analysis. FEBS Lett. 1978 Dec 15;96(2):327–330. doi: 10.1016/0014-5793(78)80428-1. [DOI] [PubMed] [Google Scholar]
  5. Brennan M. D., Weiner A. J., Goralski T. J., Mahowald A. P. The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev Biol. 1982 Jan;89(1):225–236. doi: 10.1016/0012-1606(82)90309-8. [DOI] [PubMed] [Google Scholar]
  6. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  8. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Garabedian M. J., Hung M. C., Wensink P. C. Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1396–1400. doi: 10.1073/pnas.82.5.1396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Garabedian M. J., Shepherd B. M., Wensink P. C. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell. 1986 Jun 20;45(6):859–867. doi: 10.1016/0092-8674(86)90560-x. [DOI] [PubMed] [Google Scholar]
  12. Garabedian M. J., Shirras A. D., Bownes M., Wensink P. C. The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene. 1987;55(1):1–8. doi: 10.1016/0378-1119(87)90242-3. [DOI] [PubMed] [Google Scholar]
  13. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  14. Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 1982 Nov 25;10(22):7055–7074. doi: 10.1093/nar/10.22.7055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 1981 Jan 10;9(1):r43–r74. doi: 10.1093/nar/9.1.213-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hatzopoulos P., Kambysellis M. P. Isolation and structural analysis of Drosophila grimshawi vitellogenin genes. Mol Gen Genet. 1987 Mar;206(3):475–484. doi: 10.1007/BF00428888. [DOI] [PubMed] [Google Scholar]
  17. Haymer D. S., Anleitner J. E., He M., Thanaphum S., Saul S. H., Ivy J., Houtchens K., Arcangeli L. Actin genes in the Mediterranean fruit fly, Ceratitis capitata. Genetics. 1990 May;125(1):155–160. doi: 10.1093/genetics/125.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Herskowitz I. Functional inactivation of genes by dominant negative mutations. Nature. 1987 Sep 17;329(6136):219–222. doi: 10.1038/329219a0. [DOI] [PubMed] [Google Scholar]
  19. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  20. Holmes D. S., Bonner J. Preparation, molecular weight, base composition, and secondary structure of giant nuclear ribonucleic acid. Biochemistry. 1973 Jun 5;12(12):2330–2338. doi: 10.1021/bi00736a023. [DOI] [PubMed] [Google Scholar]
  21. Hultmark D., Klemenz R., Gehring W. J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell. 1986 Feb 14;44(3):429–438. doi: 10.1016/0092-8674(86)90464-2. [DOI] [PubMed] [Google Scholar]
  22. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
  23. Jörnvall H., von Bahr-Lindström H., Jany K. D., Ulmer W., Fröschle M. Extended superfamily of short alcohol-polyol-sugar dehydrogenases: structural similarities between glucose and ribitol dehydrogenases. FEBS Lett. 1984 Jan 9;165(2):190–196. doi: 10.1016/0014-5793(84)80167-2. [DOI] [PubMed] [Google Scholar]
  24. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res. 1985 Jul 11;13(13):4971–4981. doi: 10.1093/nar/13.13.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Konsolaki M., Komitopoulou K., Tolias P. P., King D. L., Swimmer C., Kafatos F. C. 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. 1990 Apr 11;18(7):1731–1737. doi: 10.1093/nar/18.7.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mintzas A. C., Chrysanthis G., Christodoulou C., Marmaras V. J. Translation of the mRNAs coding for the major hemolymph proteins of Ceratitis capitata in cell-free system: comparison of the translatable mRNA levels to the respective biosynthetic levels of the proteins in the fat body during development. Dev Biol. 1983 Feb;95(2):492–496. doi: 10.1016/0012-1606(83)90051-9. [DOI] [PubMed] [Google Scholar]
  27. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nardelli D., Gerber-Huber S., van het Schip F. D., Gruber M., Ab G., Wahli W. Vertebrate and nematode genes coding for yolk proteins are derived from a common ancestor. Biochemistry. 1987 Oct 6;26(20):6397–6402. doi: 10.1021/bi00394a014. [DOI] [PubMed] [Google Scholar]
  29. Persson B., Bengtsson-Olivecrona G., Enerbäck S., Olivecrona T., Jörnvall H. Structural features of lipoprotein lipase. Lipase family relationships, binding interactions, non-equivalence of lipase cofactors, vitellogenin similarities and functional subdivision of lipoprotein lipase. Eur J Biochem. 1989 Jan 15;179(1):39–45. doi: 10.1111/j.1432-1033.1989.tb14518.x. [DOI] [PubMed] [Google Scholar]
  30. Postlethwait J. H., Bownes M., Jowett T. Sexual phenotype and vitellogenin synthesis in Drosophila melanogaster. Dev Biol. 1980 Oct;79(2):379–387. doi: 10.1016/0012-1606(80)90123-2. [DOI] [PubMed] [Google Scholar]
  31. Sharp P. M., Cowe E., Higgins D. G., Shields D. C., Wolfe K. H., Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res. 1988 Sep 12;16(17):8207–8211. doi: 10.1093/nar/16.17.8207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sharp P. M., Li W. H. Codon usage in regulatory genes in Escherichia coli does not reflect selection for 'rare' codons. Nucleic Acids Res. 1986 Oct 10;14(19):7737–7749. doi: 10.1093/nar/14.19.7737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  34. Staden R. Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):521–538. doi: 10.1093/nar/12.1part2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Teem J. L., Abovich N., Kaufer N. F., Schwindinger W. F., Warner J. R., Levy A., Woolford J., Leer R. J., van Raamsdonk-Duin M. M., Mager W. H. A comparison of yeast ribosomal protein gene DNA sequences. Nucleic Acids Res. 1984 Nov 26;12(22):8295–8312. doi: 10.1093/nar/12.22.8295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wallace R. B., Johnson M. J., Suggs S. V., Miyoshi K., Bhatt R., Itakura K. A set of synthetic oligodeoxyribonucleotide primers for DNA sequencing in the plasmid vector pBR322. Gene. 1981 Dec;16(1-3):21–26. doi: 10.1016/0378-1119(81)90057-3. [DOI] [PubMed] [Google Scholar]
  37. Warren T. G., Mahowald A. P. Isolation and partial chemical characterization of the three major yolk polypeptides from Drosophila melanogaster. Dev Biol. 1979 Jan;68(1):130–139. doi: 10.1016/0012-1606(79)90248-3. [DOI] [PubMed] [Google Scholar]
  38. Yan Y. L., Kunert C. J., Postlethwait J. H. Sequence homologies among the three yolk polypeptide (Yp) genes in Drosophila melanogaster. Nucleic Acids Res. 1987 Jan 12;15(1):67–85. doi: 10.1093/nar/15.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES