Skip to main content
Log in

Anterior epidermis-specific expression of the cuticle gene EDG84A is controlled by many cis-regulatory elements in Drosophila melanogaster

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

During insect metamorphosis, a pulse of ecdysteroids induces many different morphological changes depending on different parts of the body. In Drosophila, although a number of transcription factors are expressed in a stage-specific manner in response to an ecdysteroid pulse, little is known on the regulatory mechanism for space-specific gene expression during metamorphosis. The EDG84A gene encoding pupal cuticle protein is one of the targets of ecdysteroid-inducible transcription factor βFTZ-F1 and is expressed only in anterior epidermis of the body during mid- to late prepupal period, whereas βFTZ-F1 is expressed in almost all tissues. To address the regulatory mechanism of the tissue-specific expression of the EDG84A gene, we established transgenic fly lines which carry various upstream regions of the gene fused to the LacZ gene and examined the expression pattern of the reporter gene. Results of the transgenic fly reporter assays showed that the space-specific expression is controlled by at least four positive and two negative elements within a 263-bp region near the transcription start site, and at least three of them showed space-specific effects to the anterior body trunk. These results suggest that both high expression level and differential expression are achieved through many cis-regulatory elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anand S, Wang WC, Powell DR, Bolanowski SA, Zhang J, Ledje C, Pawashe AB, Amemiya CT, Shashikant CS (2003) Divergence of Hoxc8 early enhancer parallels diverged axial morphologies between mammals and fishes. Proc Natl Acad Sci U S A 100:15666–15669

    Article  PubMed  CAS  Google Scholar 

  • Apple RT, Fristrom JW (1991) 20-Hydroxyecdysone is required for, and negatively regulates, transcription of Drosophila pupal cuticle protein genes. Dev Biol 146:569–582

    Article  PubMed  CAS  Google Scholar 

  • Bayer CA, Holley B, Fristrom JW (1996a) A switch in Broad-Complex zinc-finger isoform expression is regulated post-transcriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol 177:1–14

    Article  PubMed  CAS  Google Scholar 

  • Bayer CA, von Kalm L, Fristrom JW (1996b) Gene regulation in imaginal disc and salivary gland development during Drosophila metamorphosis. In: Gilbert LI, Tata JR, Atkinson BG (eds) Metamorphosis; postembryonic reprogramming of gene expression in amphibian and insect cells. Academic, San Diego, pp 321–361

    Google Scholar 

  • Bender M, Imam FB, Talbot WS, Ganetzky B, Hogness DS (1997) Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 91:777–788

    Article  PubMed  CAS  Google Scholar 

  • Broadus J, McCabe JR, Endrizzi B, Thummel CS, Woodard CT (1999) The Drosophila bFTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol Cell 3:143–149

    Article  PubMed  CAS  Google Scholar 

  • Brodu V, Mugat B, Fichelson P, Lepesant JA, Antoniewski C (2001) A UAS site substitution approach to the in vivo dissection of promoters: interplay between the GATAb activator and the AEF-1 repressor at a Drosophila ecdysone response unit. Development 128:2593–2602

    PubMed  CAS  Google Scholar 

  • DiBello PR, Withers DA, Bayer CB, Fristrom JW, Guild GM (1991) The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics 129:385–397

    PubMed  CAS  Google Scholar 

  • Emery IF, Bedian V, Guild GM (1994) Differential expression of Broad-Complex transcription factors may forecast distinct developmental tissue fates during Drosophila metamorphosis. Development 120:3275–3287

    PubMed  CAS  Google Scholar 

  • Falb D, Maniatis T (1992) Drosophila transcriptional repressor protein that binds specifically to negative control elements in fat body enhancers. Mol Cell Biol 12:4103–4903

    Google Scholar 

  • Fechtel K, Natzle JE, Brown EE, Fristrom JW (1988) Prepupal differentiation of Drosophila imaginal discs: identification of four genes whose transcripts accumulate in response to a pulse of 20-hydroxyecdysone. Genetics 120:465–474

    PubMed  CAS  Google Scholar 

  • Fechtel K, Fristrom DK, Fristrom JW (1989) Prepupal differentiation in Drosophila: distinct cell types elaborate a shared structure, the pupal cuticle, but accumulate transcripts in unique patterns. Development 106:649–656

    PubMed  CAS  Google Scholar 

  • Fristrom D, Fristrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster, 2. Cold Spring Harbor Laboratory, New York, pp 843–898

    Google Scholar 

  • Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, Hogness DS (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Kageyama Y, Hirose S, Ueda H (1996) Regulation of the EDG84A gene by FTZ-F1 during metamorphosis in Drosophila melanogaster. Mol Cell Biol 16:6509–6515

    PubMed  CAS  Google Scholar 

  • Renault N, King-Jones K, Lehmann N (2001) Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specific hormone response. Development 128:3729–3737

    PubMed  CAS  Google Scholar 

  • Riddiford LM (1993) Hormones and Drosophila development. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster, 2. Cold Spring Harbor Laboratory, New York, pp 899–939

    Google Scholar 

  • Schubiger M, Wade AA, Carney GE, Truman JW, Bender M (1998) Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125:2053–2062

    PubMed  CAS  Google Scholar 

  • Shimada A (1996) PCR-based site-directed mutagenesis. Methods Mol Biol 57:157–165

    PubMed  CAS  Google Scholar 

  • Skaer H (1993) The alimentary canal. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster, 2. Cold Spring Harbor Laboratory, New York, pp 941–1012

    Google Scholar 

  • Talbot WS, Swyryd EA, Hogness DS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323–1337

    Article  PubMed  CAS  Google Scholar 

  • Thummel CS (1995) From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83:871–877

    Article  PubMed  CAS  Google Scholar 

  • Thummel CS (1996) Files on steroids—Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12:306–310

    Article  PubMed  CAS  Google Scholar 

  • Thummel CS, Boulet AM, Lipshitz HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74:445–450

    Article  PubMed  CAS  Google Scholar 

  • Truman JW, Talbot WS, Fahrbach SE, Hogness DS (1994) Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120:219–234

    PubMed  CAS  Google Scholar 

  • Von Kalm L, Crossgrove K, von Seggern D, Guild GM, Beckendorf SK (1994) The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J 13:3505–3516

    PubMed  Google Scholar 

  • Yamada M, Murata T, Hirose S, Lavorgna G, Suzuki E, Ueda H (2000) Temporally restricted expression of transcription factor FTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster. Development 127:5083–5092

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank all the members of our laboratory for their support and useful comments on the manuscript. We also thank Toshiyuki Takano, Masataka Okabe, Ryu Ueda, Haruhiko Fujiwara, Hiroyuki Araki, Shigeo Hayashi, and Yasushi Hiromi for critical comments and suggestions on the manuscript. This work was supported by Grants-in-aid for Scientific Research from the Ministry of Education, Science, Sports, Culture and Technology of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hitoshi Ueda.

Additional information

Communicated by C. Desplan

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kayashima, Y., Hirose, S. & Ueda, H. Anterior epidermis-specific expression of the cuticle gene EDG84A is controlled by many cis-regulatory elements in Drosophila melanogaster . Dev Genes Evol 215, 545–552 (2005). https://doi.org/10.1007/s00427-005-0013-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-005-0013-z

Keywords

Navigation