Skip to main content
Log in

Developmental regulation and complex organization of the promoter of the non-codinghsrω gene ofDrosophila melanogaster

  • Articles
  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

The nucleus-limited large non-coding hsrω-n RNA product of the93D or thehsrω gene ofDrosophila melanogaster binds to a variety of RNA-binding proteins involved in nuclear RNA processing. We examined the developmental and heat shock induced expression of this gene byin situ hybridization of nonradioactively labelled riboprobe to cellular transcripts in intact embryos, larval and adult somatic tissues of wild type and an enhancer-trap line carrying thehsrω 05241 allele due to insertion of aP-LacZ-rosy + transposon at — 130 bp position of thehsrω promoter. We also examinedLacZ expression in the enhancer-trap line and in two transgenic lines carrying different lengths of thehsrω promoter upstream of theLacZ reporter. ThehsrΩ gene is expressed widely at all developmental stages; in later embryonic stages, its expression in the developing central nervous system was prominent. In spite of insertion of a big transposon in the promoter, expression of thehsrω 05241 allele in the enhancer-trap line, as revealed byin situ hybridization to hsrω transcripts in cells, was similar to that of the wild type allele in all the embryonic, larval and adult somatic tissues examined. Expression of theLacZ gene in this enhancer-trap line was similar to that of thehsrω RNA in all diploid cell types in embryos and larvae but in the polytene cells, theLacZ gene did not express at all, neither during normal development nor after heat shock. Comparison of the expression patterns ofhsrω gene and those of theLacZ reporter gene under its various promoter regions in the enhancer-trap and transgenic lines revealed a complex pattern of regulation, which seems to be essential for its dynamically varying expression in diverse cell types.

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.

Similar content being viewed by others

Abbreviations

RISH:

RNA : RNA in situ hybridization

PSS:

Poels’ salt solution

HSE:

heat shock elements

References

  • Ausubel F M, Brent R, Kingston R E, Moore D D, Seidman J G, Smith J A and Struhl K (eds) 1994Current protocols in molecular biology Vol 2 (New York: John Wiley)

    Google Scholar 

  • Bendena W G, Ayme-Southgate A, Garbe J C and Pardue M L 1991 Expression of heat-shock locushsr-omega in non-stressed cells during development inDrosophila melanogaster;Dev. Biol. 144 65–77

    Article  PubMed  CAS  Google Scholar 

  • Bendena W G, Garbe J C, Traverse K L, Lakhotia S C and Pardue M L 1989 Multiple inducers of the Drosophila heat shock locus 93DhsrΩ: Inducer-specific patterns of the three transcripts;J. Cell Biol. 108 2017–2028

    Article  PubMed  CAS  Google Scholar 

  • Buchenau P, Saumweber H and Arndt-jovin D J 1997 The dynamic nuclear redistribution of an hnRNP K-homologous protein duringDrosophila embryo development and heat shock Flexibility of transcription sites in vivo;J. Cell Biol. 137 291–303

    Article  PubMed  CAS  Google Scholar 

  • Dequin R, Saumweber H and Sedat J W 1984 Proteins shifting from the cytoplasm into the nuclei during early embryogenesis ofDrosophila melanogaster;Dev. Biol. 104 37–48

    Article  PubMed  CAS  Google Scholar 

  • Erdmann V A, Szymanski M, Hochberg A, de Groot N and Barciszewski J 1999 Collection of mRNA-like non-coding RNAs;Nucleic Acids Res. 27 192–195

    Article  PubMed  CAS  Google Scholar 

  • Foe V E, Odell G M and Edgar B A 1993 Mitosis and morphogenesis in theDrosophila embryo: point and counterpoint; inThe development of Drosophila melanogaster (eds) M Bate and A M Arias (New York: Cold Spring Harb. Lab. Press) pp 149–300

    Google Scholar 

  • Hellmund D and Serfling E 1984 Structure of hsp70-coding genes inDrosophila; inHeat shock response of eukaryotic cells (ed) L Nover (Berlin: Springer-Verlag) pp 23–28

    Google Scholar 

  • Kelly R L and Kuroda M I 2000 The role of chromosomal RNAs in marking the X for dosage compensation;Curr. Opi. Genet. Dev. 98 513–522

    Google Scholar 

  • Lakhotia S C 1996 RNA polymerase II dependent genes that do not code for protein;Indian J. Biochem. Biophys. 33 93–102

    Google Scholar 

  • Lakhotia S C 1999 Non-coding RNAs: versatile roles in cell regulation;Curr. Sci. 77 479–480

    Google Scholar 

  • Lakhotia S C and Sharma A 1995 RNA metabolismin situ at the 93D heat shock locus in polytene nuclei ofDrosophila melanogaster after various treatments;Chromosome Res. 3 151–161

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia S C and Sharma A 1996 The 93Dhsr-omega locus ofDrosophila: non-coding gene with house keeping functions;Genetica 97 339–348

    Article  Google Scholar 

  • Lakhotia S C and Mutsuddi M 1996 Heat shock but not benzamide and colchicine response elements are present within the — 844 bp upstream of region of thehsrΩ gene ofDrosophila melanogaster;J. Biosci. 21 235–246

    Article  Google Scholar 

  • Lakhotia S C, Ray P, Rajendra T K and Prasanth K V 1999 The non-coding transcripts ofhsr-omega gene inDrosophila: Do they regulate trafficking and availability of nuclear RNA-processing factors?;Curr. Sci. 77 553–563

    CAS  Google Scholar 

  • Lakhotia S C and Tapadia M G 1998 Genetic mapping of the amide response element/s of thehsrΩ locus ofDrosophila melanogaster;Chromosoma 107 127–135

    Article  PubMed  CAS  Google Scholar 

  • Lehmann R and Tautz D 1994In situ hybridization to RNA;Methods Enzymol. 44 446–487

    Google Scholar 

  • Lindquist S 1986 The heat-shock response;Annu. Rev. Biochem. 55 1151–1191

    Article  PubMed  CAS  Google Scholar 

  • Lindsley, D L and Zimm, G G 1992The genome of Drosophila melanogaster (San Diego:Academic Press)

    Google Scholar 

  • Mukherjee T and Lakhotia S C 19793H-uridine incorporation in the puff 93D and in chromocentric heterchromatin of heat shocked salivary glands ofDrosophila melanogaster;Chromosoma 74 75–82

    Article  PubMed  CAS  Google Scholar 

  • Mutsuddi M and Lakhotia S C 1995 Spatial expression of thehsromega 93D gene in different tissues ofDrosophila melanogaster and identification of promoter elements controlling its developmental expression;Dev. Genet. 17 303–311

    Article  PubMed  CAS  Google Scholar 

  • Prasanth K V, Rajendra T K, Lal A K and Lakhotia S C 2000 Omega speckles — a novel class of nuclear speckles containing hnRNPs associated with non-coding hsr-omega RNA inDrosophila;J. Cell Sci. 113 3485–3497

    PubMed  CAS  Google Scholar 

  • Salz H K, Maine E M, Keyes L N, Samuels M E, Cline T W and Schedl P 1989 TheDrosophila female-specific sex-determination gene,Sex-lethal, has stage-, tissue- and sex-specific RNAs suggesting multiple modes of regulation;Gene Dev. 3 708–719

    Article  PubMed  CAS  Google Scholar 

  • Samuels M E, Bopp D, Colvin R A, Roscigno R F, Garcia-Blanco M A and Schedl P 1994 RNA binding by Sxl proteinsin vitro andin vivo;Mol. Cell. Biol. 14 4975–4990

    PubMed  CAS  Google Scholar 

  • Segalat L and Lepesant J A 1992 Spatial distribution of the Sm antigen inDrosophila early embryos;Biol. Cell. 75 181–185

    Article  PubMed  CAS  Google Scholar 

  • Sharma A and Lakhotia S C 1995In situ quantification of hsp70 and alpha-beta transcripts at 87A and 87C loci in relation tohsr-omega gene activity in polytene cells ofD. melanogaster;Chromosome Res. 3 386–393

    Article  PubMed  CAS  Google Scholar 

  • Spradling A C, Stern D M, Kiss I, Roote J, Laverty T and Rubin G M 1995 Gene disruptions using P transposable elements: an integral component of theDrosophila genome project;Proc. Natl. Acad. Sci. USA 92 10824–10830

    Article  PubMed  CAS  Google Scholar 

  • Spusta S C and Goldman M A 1999XISTential wanderings: The role of XIST RNA in X-chromosome inactivation;Curr. Sci. 77 530–538

    CAS  Google Scholar 

  • Wu C, Clos J, Giorgi G, Haroun R I, Kim S-J, Rabindran S K, Westwood J T, Wisniewski J and Yim G 1994 Structure and regulation of heat shock transcription factor inThe biology of heat shock proteins and molecular chaperones (eds) R I Morimoto, A Tissieres and C Georgopoulos (New York: Cold Spring Harb. Lab. Press) pp 395–416

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. C. Lakhotia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lakhotia, S.C., Rajendra, T.K. & Prasanth, K.V. Developmental regulation and complex organization of the promoter of the non-codinghsrω gene ofDrosophila melanogaster . J Biosci 26, 25–38 (2001). https://doi.org/10.1007/BF02708978

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02708978

Keywords

Navigation