Skip to main content
SpringerLink
Log in

The boll weevil vitellogenin gene: Nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes

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

Summary

Boll weevil (Anthonomus grandis) eggs contain two yolk proteins, YP47 and YP160. Using anti-YP160 antiserum as probe, a partial-length complementary DNA (cDNA) was isolated from a λgt11 adult female cDNA library. A second partial-length cDNA was isolated from a λgt 10 adult female cDNA library by differential screening with male vs. female cDNAs. Northern blot analysis showed that each cloned cDNA hybridized to a 6-kb female-specific transcript. These cDNAs were used to probe a genomic library, and two overlapping genomic clones were obtained that span the boll weevil vitellogenin gene. The entire transcription unit was sequenced, and introns were mapped by a combination of primer extension experiments, S 1 nuclease protection experiments, and polymerase chain reaction-mediated synthesis of two additional cDNA clones. Based on these data, the vitellogenin mRNA is 5511 nucleotides [plus a poly(A) tail of undetermined length] and specifies a provitellogenin of 1790 amino acids. The deduced protein has a Glu + Gln content of 16.3%, which is a relatively high value that is typical of most vitellogenins. Protein sequence similarities including Cys clusters conserved between boll weevil vitellogenin and Xenopus laevis A2 or Caenorhabditis elegans vit-5 vitellogenins indicated that the boll weevil protein is a member of the ancient nematode-vertebrate vitellogenin family. Moreover, the six introns in the boll weevil vitellogenin gene interrupt the coding region at positions closely or exactly corresponding to a subset of the position, of the 34 vertebrate vitellogenin introns, further supporting the argument for a common evolutionary relationship. This report represents the first complete nucleotide sequence and structural analysis of a nondipteran insect vitellogenin gene.

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

  • Bartlett AC (1967) Genetic markers in the boll weevil. J Hered 58:159–163

    Google Scholar 

  • Benton WD, Davis RW (1978) Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196:180–182

    Google Scholar 

  • Berger SL, Kimmel AR (1987) Guide to molecular cloning techniques. Academic Press, New York

    Google Scholar 

  • Bingham PM, Chou T-B, Mims I, Zachar Z (1988) On/off regulation of gene expression at the level of splicing. Trends Genet 4:134–138

    Google Scholar 

  • Bownes M (1986) Expression of the genes coding for vitellogenin (yolk protein). Annu Rev Entomol 31:507–531

    Google Scholar 

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

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Google Scholar 

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

    Google Scholar 

  • Byrne BM, Gruber M, AB G (1989) The evolution of egg yolk proteins. Prog Biophys Mol Biol 53:33–69

    Google Scholar 

  • Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299

    Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    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 

  • Dhadialla TS, Raikhel AS (1990) Biosynthesis of mosquito vitellogenin. J Biol Chem 265:9924–9933

    Google Scholar 

  • Doolittle RF (1987) Of Urfs and Orfs: a primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley CA

    Google Scholar 

  • Doolittle RF (1990) Searching through sequence databases. In: Doolittle RF (ed) Methods in enzymology, vol 183. Academic Press, New York, pp 99–110

    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 

  • Gemmill RM, Hamblin M, Glaser RL, Racioppi JV, Marx JL, White BN, Calvo JM, Wolfner MF, Hagedorn HH (1986) Isolation of mosquito vitellogenin genes and induction of expression by 20-hydroxyecdysone. Insect Biochem 16:761–774

    Google Scholar 

  • Gerber-Huber S, Nardelli D, Haefliger J-A, Cooper DN, Givel F, Germond J-E, Engel J, Green NM, Wahli W (1987) Precursor-product relationship between vitellogenin and the yolk proteins as derived from the complete sequence of a Xenopus vitellogenin gene. Nucleic Acids Res 15:4737–4760

    Google Scholar 

  • Gubler U, Hoffman BJ (1983) A simple and very efficient method for generating cDNA libraries. Gene 25:263–269

    Google Scholar 

  • Harnish DG, White BN (1982) An evolutionary model for the insect vitellins. J Mol Evol 18:405–413

    Google Scholar 

  • Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359

    Google Scholar 

  • Hovemann B, Galler R, Walldorf U, Kupper H, Bautz EKF (1981) Vitellogenin in Drosophila melanogaster: sequence of the yolk protein 1 gene and its flanking regions. Nucleic Acids Res 9:4721–4734

    Google Scholar 

  • Hung M-C, Wensink PC (1983) Sequence and structure conservation in yolk proteins and their genes. J Mol Biol 164: 481–492

    Google Scholar 

  • Jendrisak J, Young RA, Engel JD (1987) Cloning cDNA into λgt10 and λgt11. In: Berger SL, Kimmel AR (eds) Methods in enzymology, vol 152. Academic Press, New York, pp 359–371

    Google Scholar 

  • Kozak M (1989) The scanning model for translation: an update. J Cell Biol 108:229–241

    Google Scholar 

  • Kunkel JG, Nordin JH (1985) Yolk proteins. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, New York, pp 83–111

    Google Scholar 

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

    Google Scholar 

  • Lehrach H, Diamond D, Woznay JM, Boedtker H (1977) RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry 16:4743–4751

    Google Scholar 

  • Locke J, White BN, Wyatt GR (1987) Cloning and 5′ end nucleotide sequences of two juvenile hormone-inducible vitellogenin genes of the African migratory locust. DNA 6:331–342.

    Google Scholar 

  • Maitre J-L, Mercier L, Dolo L, Valotaire L (1985) Caracterisation de recepteurs specifiques a l'oestradiol, induction de la vitellogenine et de son mRNA dans le foie de truite arcenciel (Salmo gairdnerii). Biochimie 67:215–225

    Google Scholar 

  • Messing J (1983) New M13 vectors for cloning. In: Wu R, Grossman L, Moldave K (eds) Methods in enzymology, vol 101. Academic Press, New York, pp 20–78

    Google Scholar 

  • Nardelli D, Gerber-Huber S, van het Schip FD, Gruber M, AB G, Wahli W (1987) Vertebrate and nematode genes coding for yolk proteins are derived from a common ancestor. Biochemistry 26:6397–6402

    Google Scholar 

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

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    Google Scholar 

  • Sharrock WJ (1984) Cleavage of two yolk proteins from a precursor in C. elegans. J Mol Biol 174:419–431

    Google Scholar 

  • Shyu A-B, Raff RA, Blumenthal T (1986) Expression of the vitellogenin gene in female and male sea urchin. Proc Natl Acad Sci USA 83:3865–3869

    Google Scholar 

  • Shyu A-B, Blumenthal T, Raff RA (1987) A single gene encoding vitellogenin in the sea urchin Strongylocentrotus purpuratus: sequence at the 5′ end. Nucleic Acids Res 15:10405–10417

    Google Scholar 

  • Singh L, Jones KW (1984) The use of heparin as a simple cost-effective means of controlling background in nucleic acid hybridization procedures. Nucleic Acids Res 12:5627–5638

    Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    Google Scholar 

  • Spieth J, Blumenthal T (1985) The Caenorhabditis elegans vitellogenin gene family includes a gene encoding a distantly related protein. Mol Cell Biol 5:2495–2501

    Google Scholar 

  • Spieth J, Denison K, Zucker E, Blumenthal T (1985) The nucleotide sequence of a nematode vitellogenin gene. Nucleic Acids Res 13:7129–7137

    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 

  • Terpstra P, AB G (1988) Homology of Drosophila yolk proteins and the triacylglycerol lipase family. J Mol Biol 202:663–665

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Trewitt PM, Saffarini DA, Bergtrom G (1988) Multiple clustered genes of the haemoglobin VIIB subfamily of Chironomus thummi thummi (Diptera). Gene 69:91–100

    Google Scholar 

  • von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4690

    Google Scholar 

  • Wahli W (1988) Evolution and expression of vitellogenin genes. Trends Genet 4:227–232

    Google Scholar 

  • Wahli W, Ryffel GU (1985) Xenopus vitellogenin genes. In: MacLean N (ed) Oxford surveys on eukaryotic genes, vol 2. Oxford University Press, Oxford, pp 96–120

    Google Scholar 

  • Wang S-Y, Williams DL (1982) Biosynthesis of the vitellogenins: identification and characterization of nonphosphorylated precursors to avian vitellogenin I and vitellogenin II. J Biol Chem 257:3837–3846

    Google Scholar 

  • Wang S-Y, Smith DE, Williams DL (1983) Purification ofavian vitellogenin III: comparison with vitellogenins I and II. Biochemistry 22:6206–6212

    Google Scholar 

  • Wheeler DE, Kawooya JK (1990) Purification and characterization of honey bee vitellogenin. Arch Insect Biochem Physiol 14:253–267

    Google Scholar 

  • Wyatt GR (1988) Vitellogenin synthesis and the analysis of juvenile hormone action in locust fat body. Can J Zool 66: 2600–2610

    Google Scholar 

  • Yamamoto KR, Alberts BM, Benzinger R, Lawhorne L, Trieber G (1970) Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 40:734–744

    Google Scholar 

  • Yan YL, Kunert CJ, Postlethwait JH (1987) Sequence homologies among the three yolk polypeptide (Yp) genes in Drosophila melanogaster. Nucleic Acids Res 15:67–85

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology Department, Marquette University, 53233, Milwaukee, WI, USA

    Patrick M. Trewitt & A. Krishna Kumaran

  2. US Department of Agriculture, Biosciences Research Laboratory, 58105, Fargo, ND, USA

    Larry J. Heilmann & S.S. Degrugillier

Authors
  1. Patrick M. Trewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larry J. Heilmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S.S. Degrugillier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Krishna Kumaran
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Offprint requests to: A. Krishna Kumaran

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trewitt, P.M., Heilmann, L.J., Degrugillier, S. et al. The boll weevil vitellogenin gene: Nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes. J Mol Evol 34, 478–492 (1992). https://doi.org/10.1007/BF00160462

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160462

Key Words

Search

Navigation