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The winged-helix transcription factor JUMU is a haplo-suppressor/triplo-enhancer of PEV in various tissues but exhibits reverse PEV effects in the brain of Drosophila melanogaster

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Abstract

Gene expression goes along with changes in chromatin structure and is regulated by chromatin-modifying factors. If genes are transposed from their euchromatic position to the vicinity of heterochromatin, their expression can underly a position effect variegation (PEV). In Drosophila melanogaster a few genes are known that function in a gene dose-dependent manner as haplo-suppressors and triplo-enhancers of PEV or vice versa. The gene jumeaux (jumu) encodes a winged-helix transcription factor of multiple regulatory functions. A novel PEV test system for Drosophila melanogaster reveals that JUMU behaves as a haplo-suppressor/triplo-enhancer in different larval and adult tissues, but surprisingly behaves in the reverse manner as a haplo-enhancer/triplo-suppressor in larval and adult brains. Like jumu, the Su(var)3-9 gene also behaves as a haplo-suppressor/triplo-enhancer, but in our test system does not show any PEV effect in the brains.

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Abbreviations

CNS:

central nervous system

Dom:

Domina, synonym of the jumeaux gene

Gal4:

Gal4 transcription factor of yeast

GFP:

green fluorescent protein

HP1:

heterochromatin protein 1

Hip:

HP1-interacting protein

Hsp:

heatshock promoter

JUMU:

protein encoded by jumeaux (jumu)

PEV:

position effect variegation

Su(var):

suppressor of variegation

UAS:

upstream activating sequence

References

  • Bellen HJ, O’Kane CJ, Wilson C et al (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3:1288–1300

    Article  PubMed  CAS  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    PubMed  CAS  Google Scholar 

  • Cheah PY, Chia W, Yang X (2000) Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates. Development 127:3325–3335

    PubMed  CAS  Google Scholar 

  • Cleard F, Delattre M, Spierer P (1997) SU(VAR)3–7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation. EMBO J 16:5280–5288

    Article  PubMed  CAS  Google Scholar 

  • Dorn R, Szidonya J, Korge G et al (1993) P transposon-induced dominant enhancer mutations of position-effect variegation in Drosophila melanogaster. Genetics 133:279–290

    PubMed  CAS  Google Scholar 

  • Eissenberg JC, James TC, Foster-Hartnett DM V et al (1990) Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A 87:9923–9927

    Article  PubMed  CAS  Google Scholar 

  • Eissenberg JC, Morris GD, Reuter G, Hartnett T (1992) The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics 131:345–352

    PubMed  CAS  Google Scholar 

  • Giot L, Bader JS, Brouwer C et al (2003) A protein interaction map of Drosophila melanogaster. Science 302:1727–1736

    Article  PubMed  CAS  Google Scholar 

  • Gregory SL, Shandala T, O’Keefe L, Jones L, Murray MJ, Saint R (2007) A Drosophila overexpression screen for modifiers of Rho signalling in cytokinesis. Fly 1:13–22

    PubMed  Google Scholar 

  • Heitz E (1928) Das Heterochromatin der Moose. Jb Wiss Bot 69:728–818

    Google Scholar 

  • Henikoff S (1996) Dosage-dependent modification of position-effect variegation in Drosophila. BioEssays 18:401–409

    Article  PubMed  CAS  Google Scholar 

  • Kearney JB, Wheeler SR, Estes P, Crews ST (2004) Gene expression profiling of the developing Drosophila CNS midline cells. Dev Biol 275:473–492

    Article  PubMed  CAS  Google Scholar 

  • Lindsley DT, Zimm GG (1992) The Genome of Drosophila melanogaster. Academic Press, San Diego

    Google Scholar 

  • Locke J, Kotarski MA, Tartof KD (1988) Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics 120:181–198

    PubMed  CAS  Google Scholar 

  • Lu BY, Bishop CP, Eissenberg JC (1996) Developmental timing and tissue specificity of heterochromatin-mediated silencing. EMBO J 15:1323–1332

    PubMed  CAS  Google Scholar 

  • Lu BY, Ma J, Eissenberg JC (1998) Developmental regulation of heterochromatin-mediated gene silencing in Drosophila. Development 125:2223–2234

    PubMed  CAS  Google Scholar 

  • Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373

    Article  PubMed  CAS  Google Scholar 

  • Muller HJ (1930) Types of visible variations induced by X-rays in Drosophila. J Genet 22:299–334

    Article  Google Scholar 

  • Patel NH (1994) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. In: Goldstein LSB, Fyrberg EA (eds.) Methods in Cell Biology, Vol. 44. Academic Press, pp. 445–487

  • Reuter G, Szidonya J (1983) Cytogenetic analysis of variegation suppressors and a dominant temperature-sensitive lethal in region 23–26 of chromosome 2L in Drosophila melanogaster. Chromosoma 88:277–285

    Article  PubMed  CAS  Google Scholar 

  • Reuter G, Wolff I (1981) Isolation of dominant suppressor mutations for position-effect variegation in Drosophila melanogaster. Mol Gen Genet 182:516–519

    Article  PubMed  CAS  Google Scholar 

  • Reuter G, Hoffmann HJ, Wolff I (1983) Genetic study of position-effect variegation in Drosophila melanogaster: In(1)wm4h as a standard rearrangement for the isolation and characterization of suppressor and enhancer mutants. Biol Zbl 102:281–298

    Google Scholar 

  • Reuter G, Wolff I, Friebe B (1985) Functional properties of the heterochromatic sequences inducing wm4 position-effect variegation in Drosophila melanogaster. Chromosoma 93:132–139

    Article  Google Scholar 

  • Reuter G, Dorn R, Wustmann G, Friebe B, Rauh G (1986) Third chromosome suppressor of position-effect variegation loci in Drosophila melanogaster. Mol Gen Genet 202:481–487

    Article  CAS  Google Scholar 

  • Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489–500

    Article  PubMed  CAS  Google Scholar 

  • Rudolph T, Yonezawa M, Lein S et al (2007) Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3–3. Mol Cell 26:103–115

    Article  PubMed  CAS  Google Scholar 

  • Schotta G, Ebert A, Krauss V et al (2002) Central role of Drosophila SU(VAR)3–9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21:1121–1131

    Article  PubMed  CAS  Google Scholar 

  • Schotta G, Ebert A, Dorn R, Reuter G (2003) Position-effect variegation and the genetic dissection of chromatin regulation in Drosophila. Semin Cell Dev Biol 14:67–75

    Article  PubMed  CAS  Google Scholar 

  • Schwendemann A, Matkovic T, Linke C, Klebes A, Hofmann A, Korge G (2008) Hip, an HP1-interacting protein, is a haplo- and triplo-suppressor of position effect variegation. Proc Natl Acad Sci U S A 105:204–209

    Article  PubMed  CAS  Google Scholar 

  • Seum C, Spierer A, Pauli D et al (1996) Position-effect variegation in Drosophila depends on dose of the gene encoding the E2F transcriptional activator and cell cycle regulator. Development 122:1949–1956

    PubMed  CAS  Google Scholar 

  • Siegmund T, Korge G (2001) Innervation of the ring gland of Drosophila melanogaster. J Comp Neurol 431:481–491

    Article  PubMed  CAS  Google Scholar 

  • Spofford JB (1976) Position-effect variegation in Drosophila. In: Ashburner M, Novitski E (eds) The Genetics and Biology of Drosophila. Academic Press, New York, pp 955–1018

    Google Scholar 

  • Stroedicke M, Karberg S, Korge G (2000) Domina (Dom), a new Drosophila member of the FKH/WH gene family, affects morphogenesis and is a suppressor of position-effect variegation. Mech Dev 96:67–78

    Article  Google Scholar 

  • Sugimura I, Adachi-Yamada T, Nishi Y, Nishida Y (2000) A Drosophila Winged-helix nude (Whn)-like transcription factor with essential functions throughout development. Dev Growth Differ 42:237–248

    Article  PubMed  CAS  Google Scholar 

  • Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G (1994) The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3–9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13:3822–3831

    PubMed  CAS  Google Scholar 

  • van de Flierdt K (1975) No multistrandedness in mitotic chromosomes of Drosophila melanogaster. Chromosoma 50:431–434

    Article  PubMed  Google Scholar 

  • Wallrath LL, Elgin SC (1995) Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev 9:1263–1277

    Article  PubMed  CAS  Google Scholar 

  • Wilson C, Pearson RK, Bellen HJ et al (1989) P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev 3:1301–1313

    Article  PubMed  CAS  Google Scholar 

  • Zhimulev IF, Belyaeva ES (2003) Intercalary heterochromatin and genetic silencing. Bioessays 25:1040–1051

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Gunter Reuter (Martin-Luther-Universität, Halle) for the anti-SU(VAR)3-9 antibodies and for providing the Su(var)3–9 06 fly stock.

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Correspondence to Günter Korge.

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Responsible Editor: Walther Traut.

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Hofmann, A., Brünner, M. & Korge, G. The winged-helix transcription factor JUMU is a haplo-suppressor/triplo-enhancer of PEV in various tissues but exhibits reverse PEV effects in the brain of Drosophila melanogaster . Chromosome Res 17, 347–358 (2009). https://doi.org/10.1007/s10577-009-9026-1

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  • DOI: https://doi.org/10.1007/s10577-009-9026-1

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