Skip to main content
SpringerLink
Log in

Genetic elements near the structural gene modulate the level of dopa decarboxylase during Drosophila development

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

Summary

Measurement of dopa decarboxylase (DDC) levels in 109 strains of Drosophila melanogaster isogenic for second chromosomes isolated independently from natural populations was undertaken. One of the most extreme variants, designated Ddc +4, was shown to have about 20% more DDC activity at adult eclosion than a standard laboratory strain used for comparison. The DDC overproduction was shown to segregate with the second chromosome and was mapped to a position within 0.15 map units of the DDC structural gene. The variant was shown to be an underproducer of DDC activity at pupariation and the genetic element responsible for this trait mapped in an identical fashion to that causing overproduction. The temporal phenotype described above was observed in the epidermis but DDC activity levels in neural tissue were normal. Examination of CRM levels at pupariation and eclosion revealed that altered DDC protein levels were responsible for the variant DDC activity levels. Electrophoretic analysis under both denaturing and non-denaturing conditions indicated that the DDC molecules in Ddc +4 and the laboratory strain were indistinguishable. These results suggest that alterations in a genetic element (or elements) lying in close proximity to the structural gene are responsible for the complex temporal phenotype of DDC activity exhibited in the variant Ddc +4.

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

Abbreviations

CRM:

cross-reacting material

DDC:

dopa decarboxylase

PTU:

phenylthiourea

References

  • Abraham I, Doane W (1978) Genetic regulation of tissue-specific expression of amylase structural genes in Drosophila melanogaster. Proc Natl Acad Sci USA 75:4446–4450

    Google Scholar 

  • Affara NA, Robert B, Jacquet M, Buckingham ME, Gros F (1980) Changes in gene expression during myogenic differentiation. I. Regulation of messenger RNA sequences expressed during myotube formation. J Mol Biol 140:441–458

    Google Scholar 

  • Ashburner M, Chihara C, Meltzer P, Richards G (1974) Temporal control of puffing activity in polytene chromosomes. Cold Spring Harbor Symposia on Quantitive Biology 38:655–662

    Google Scholar 

  • Bernstein S, Donady J (1980) RNA synthesis and coding capacity of polyadenylated and nonpolyadenylated mRNA from cultures of differentiating Drosophila melanogaster myoblasts. Dev Biol 79:288–398

    Google Scholar 

  • Bewley GC (1978) Heat stability studies at the α-glycerolphosphate dehydrogenase locus in populations of Drosophila melanogasten. Biochem Genet 16:769–775

    Google Scholar 

  • Bewley GC (1981) Genetic control of the developmental program of L-glycerol-3-phosphate dehydrogenase isozymes in Drosophila melanogaster: identification of a cis-acting temporal element affecting GPDH-3 expression. Dev Genet 2:113–129

    Google Scholar 

  • Biessman H (1981) Changes in the abundance of polyadenylated RNAs in development of Drosophila melanogaster analyzed with cloned DNA fragments. Dev Biol 83:62–68

    Google Scholar 

  • Bigelis R, Burridge K (1978) The immunological detection of yeast nonsense termination fragments on sodium dodecylsulfate-polyacrylamide gels Biochem Biophys Res Comm 82:322–327

    Google Scholar 

  • Bodenstein D (1950) The post-embryonic development of Drosophila. In: Demerec M (ed) The biology of Drosophia Wiley, New York

    Google Scholar 

  • Clark WC, Pass, PS, Venkataraman B, Hodgetts RB (1978) Dopadecarboxylase from Drosophila melanogaster: purification, characterization and an analysis of mutants. Mol Gen Genet 162:287–297

    Google Scholar 

  • Davidson E, Britten R (1979) Regulation of gene expression: possible role of repetitive sequences. Science 204:1052–1059

    Google Scholar 

  • Dickinson WJ, Carson HL (1979) Regulation of the tissue specificity of an enzyme by a cis-acting genetic element: evidence from interspecific Drosophila hybrids. Proc Natl Acad Sci USA 76:4559–4562

    Google Scholar 

  • Donahue TF, Farabaugh PJ, Fink GR (1982) The nucleotide sequence of the His-4 region of yeast. Gene 18:47–59

    Google Scholar 

  • Ephrussi B, Beadle GW (1936) A technique for transplantation for Drosophila. Am Nat 70:218–225

    Google Scholar 

  • Hirsh J, Davidson N (1981) Isolation and characterization of the dopa decarboxylase gene of Drosophila melanogaster. Mol Cell Biol 1:475–485

    Google Scholar 

  • Kessler SW (1976) Cell membrane antigen isolation with the staphylococcal protein A-antibody absorbent. J Immunol 117:1482–1489

    Google Scholar 

  • Kikuchi Y, King J (1975) Genetic control of bacteriophage T4 baseplate morphogenesis. I. Sequential assembly of the major precursor, in vivo and in vitro. J Mol Biol 99:645–672

    Google Scholar 

  • King JJ, McDonald JF (1983) Genetic localization and biochemical characterization of a trans-acting regulatory effect in Drosophila. Genetics 105:55–69

    Google Scholar 

  • Kraminsky GP, Clark WC, Estelle MA, Gietz RD, Sage BA, O'Connor JD, Hodgetts RB (1980) Induction of translatable mRNA for dopa decarboxylase in Drosophila: an early response to ecdysterone. Proc Natl Acad Sci USA 77:4175–4179

    Google Scholar 

  • Laurie-Ahlberg CC, Wilton AN, Curtsinger JW, Emigh TH (1982) Naturally occurring activity variation in Drosophila melanogaster. I. Sources of variation for 23 enzymes. Genetics 102:191–206

    Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst Wash Publ No. 627

  • Lowry OH, Rosebrough NJ, Farr AI, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–269

    Google Scholar 

  • McCaman MW, McCaman RE, Lees GJ (1972) Liquid cation exchange-a basis for sensitive radiometric assays for aromatic amino acid decarboxylases. Anal Biochem 45:242–252

    Google Scholar 

  • McCarron M, O'Donnell J, Chovnick A, Bhellar BS, Hewitt J, Candido EPM (1979). Organization of the rosy locus in Drosophila melanogaster further evidence in support of cis-acting control elements. Genetics 91:275–293

    Google Scholar 

  • Nash DN 1963 PhD Thesis, Cambridge University

  • Nash DN, Bell JB (1968) Larval age and the pattern of DNA synthesis in polytene chromosomes. Can J Genet Cytol 10:82–92

    Google Scholar 

  • Nasmyth KA (1982) The regulation of yeast mating-type chromatin structure by Sir: an action at a distance affecting both transcription and transposition. Cell 30:567–578

    Google Scholar 

  • Paigen K (1979) Acid hydrolases as models as genetic control. In: Roman HL, Campbell A, Sandler LM (eds) Ann Rev Genet 13:419–466

  • Rabinow L, Dickinson WJ (1981) A cis-acting regulator of enzyme tissue specificity in Drosophila is expressed at the RNA level. Mol Gen Genet 183:264–269

    Google Scholar 

  • Sakoyama Y, Okuba S (1981) Two-dimensional gel patterns of protein species during development of Drosophila embryos. Dev Biol 81:361–365

    Google Scholar 

  • Scandalios JG, Chang DY, McMillin DE, Tsaftaris A, Moll RH (1980) Genetic regulation of the catalase developmental program in maize scutellum: identification of a temporal regulatory gene. Proc Natl Acad Sci USA 77:5360–5364

    Google Scholar 

  • Sherman F, Cardillo TS, Errede B, Friedman L, McKnight G, Stiles J (1981) Yeast mutants overproducing iso-cytochromes c. In: von Wettstein J, Friis J, Kielland-Brandt M, Stenderup A (eds) Molecular genetics in yeast. Munksgaard, Copenhagen

    Google Scholar 

  • Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germline chromosomes. Science 218:341–347

    Google Scholar 

  • Swank RT, Paigen K, Ganschow RE (1973) Genetic control of glucuronidase induction in mice. J Mol Biol 81:225–243

    Google Scholar 

  • Wright TRF (1976) The genetics of dopa decarboxylase and α-methyl dopa sensitivity in Drosophila melanogaster. Am Zool 17:707–721

    Google Scholar 

  • Wright TRF, Bewley GC, Sherald AF (1976) The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopa decarboxylase deficient mutants and their relationship to the α-methyl dopa hypersensitive mutants. Genetics 84:287–310

    Google Scholar 

  • Wright TRF, Black BC, Bishop CP, Marsh JL, Pentz R, Wright EY (1982) The genetics of dopa decarboxylase in Drosophila melanogaster. V. Ddc and 1(2) amd alleles; isolation, characterization and intragenic complementation. Mol Gen Genet 188:18–26

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, University of Alberta, T6G 2E9, Edmonton, Alberta, Canada

    Mark A. Estelle & Ross B. Hodgetts

Authors
  1. Mark A. Estelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ross B. Hodgetts
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by W. Gehring

Rights and permissions

Reprints and permissions

About this article

Cite this article

Estelle, M.A., Hodgetts, R.B. Genetic elements near the structural gene modulate the level of dopa decarboxylase during Drosophila development. Mol Gen Genet 195, 434–441 (1984). https://doi.org/10.1007/BF00341444

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00341444

Keywords

Search

Navigation