Skip to main content
SpringerLink
Log in

Drosophila under the lens: imaging from chromosomes to whole embryos

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Microscopy has been a very powerful tool for Drosophila research since its inception, proving to be essential for the evaluation of mutant phenotypes, the understanding of cellular and tissue physiology, and the illumination of complex biological questions. In this article we review the breadth of this field, making note of some of the seminal papers. We expand on the use of microscopy to study questions related to gene locus and nuclear architecture, presenting new data using fluorescence in-situ hybridization techniques that demonstrate the flexibility of Drosophila chromosomes. Finally, we review the burgeoning use of fluorescence in-vivo imaging methods to yield quantitative information about cellular processes.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • Ahmad K, Henikoff S (2001) Centromeres are specialized replication domains in heterochromatin. J Cell Biol 153: 101–110.

    Article  PubMed  CAS  Google Scholar 

  • Amrein H, Axel R (1997) Genes expressed in neurons of adult male Drosophila. Cell 88: 459–469.

    Article  PubMed  CAS  Google Scholar 

  • Ando R, Mizuno H, Miyawaki A (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306: 1370–1373.

    Article  PubMed  CAS  Google Scholar 

  • Arnoldus EPJ, Peters ACB, Bots GTAM et al. (1989) Somatic pairing of chromosome 1 centromeres in interphase nuclei of human cerebellum. Hum Genet 83: 231–234.

    Article  PubMed  CAS  Google Scholar 

  • Arnoldus EPJ, Noordermeer IA, Peters ACB et al. (1991) Interphase cytogenetics reveals somatic pairing of chromosome 17 centromeres in normal human brain tissue, but no trisomy 7 or sex-chromosome loss. Cytogenet Cell Genet 56: 214–216.

    PubMed  CAS  Google Scholar 

  • Bantignies F, Grimaud C, Lavrov S et al. (2003) Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 17: 2406–2420.

    Article  PubMed  CAS  Google Scholar 

  • Belmont A (2003) Dynamics of chromatin, proteins, and bodies within the cell nucleus. Curr Opin Cell Biol 15: 304–310.

    Article  PubMed  CAS  Google Scholar 

  • Beuchle D, Struhl G, Muller J (2001) Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128: 993–1004.

    PubMed  CAS  Google Scholar 

  • Bornfleth H, Edelmann P, Zink D et al. (1999) Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy. Biophys J 77: 2871–2886.

    Article  PubMed  CAS  Google Scholar 

  • Bossing T, Technau GM (1994) The fate of the cns midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120: 1895–1906.

    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 

  • Bratu DP, Cha BJ, Mhlanga MM et al. (2003) Visualizing the distribution and transport of mRNAs in living cells. Proc Natl Acad Sci USA 100: 13308–13313.

    Article  PubMed  CAS  Google Scholar 

  • Bridges C (1935) Salivary chromosome maps: with a key to the banding of the chromosomes of Drosophila melanogaster. 26: 60–64.

  • Brown KE, Baxter J, Graf D et al. (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207–217.

    Article  PubMed  CAS  Google Scholar 

  • Buchenau P, Saumweber H, Arndt-Jovin DJ (1993) Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning microscopy. J Cell Sci 104: 1175–1185.

    PubMed  CAS  Google Scholar 

  • Buchenau P, Saumweber H, Arndt-Jovin DJ (1997) The dynamic nuclear redistribution of an hnRNP K-homologous protein during Drosophila embryo development and heat shock. Flexibility of transcription sites in vivo. J Cell Biol 137: 291–303.

    Article  PubMed  CAS  Google Scholar 

  • Casso D, Ramirez-Weber FA, Kornberg TB (1999) GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev 88: 229–232.

    Article  PubMed  CAS  Google Scholar 

  • Chalfie M, Tu Y, Euskirchen G et al. (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802–805.

    PubMed  CAS  Google Scholar 

  • Chen S, Corces VG (2001) The gypsy insulator of Drosophila affects chromatin structure in a directional manner. Genetics 159: 1649–1658.

    PubMed  CAS  Google Scholar 

  • Cheutin T, McNairn AJ, Jenuwein T et al. (2003) Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299: 721–725.

    Article  PubMed  CAS  Google Scholar 

  • Chubb JR, Boyle S, Perry P, Bickmore WA (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12: 439–445.

    Article  PubMed  CAS  Google Scholar 

  • Clarkson M, Saint R (1999) A His2AvDGFP fusion gene complements a lethal His2AvD mutant allele and provides an in vivo marker for Drosophila chromosome behavior. DNA Cell Biol 18: 457–462.

    Article  PubMed  CAS  Google Scholar 

  • Csink A, Henikoff S (1996) Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381: 529–531.

    Article  PubMed  CAS  Google Scholar 

  • Csink AK, Henikoff S (1998) Large-scale chromosomal movements during interphase progression in Drosophila. J Cell Biol 143: 13–22.

    Article  PubMed  CAS  Google Scholar 

  • Dernburg AF, Broman KW, Fung JC et al. (1996) Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85: 745–759.

    Article  PubMed  CAS  Google Scholar 

  • Dietzel S, Niemann H, Bruckner B et al. (1999) The nuclear distribution of Polycomb during Drosophila melanogaster development shown with a GFP fusion protein. Chromosoma 108: 83–94.

    Article  PubMed  CAS  Google Scholar 

  • Drysdale RA, Crosby MA (2005) FlyBase: genes and gene models. Nucleic Acids Res 33: D390–D395.

    Article  PubMed  CAS  Google Scholar 

  • Ficz G, Heintzmann R, Arndt-Jovin DJ (2005) Polycomb group protein complexes exchange rapidly in living Drosophila. Development 132: 3963–3976.

    Article  PubMed  CAS  Google Scholar 

  • Foe V (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107: 1–22.

    PubMed  CAS  Google Scholar 

  • Fung JC, Marshall WF, Dernburg A et al. (1998) Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J Cell Biol 141: 5–20.

    Article  PubMed  CAS  Google Scholar 

  • Furlong EE, Andersen EC, Null B et al. (2001a) Patterns of gene expression during Drosophila mesoderm development. Science 293: 1629–1633.

    Article  PubMed  CAS  Google Scholar 

  • Furlong EE, Profitt D, Scott MP (2001b) Automated sorting of live transgenic embryos. Nat Biotechnol 19: 153–156.

    Article  PubMed  CAS  Google Scholar 

  • Gemkow MJ, Verveer PJ, Arndt-Jovin DJ (1998) Homologous association of the Bithorax-Complex during embryogenesis: consequences for transvection in Drosophila melanogaster. Development 125: 4541–4552.

    PubMed  CAS  Google Scholar 

  • Georgiev PG, Corces VG (1995) The SU(HW) protein bound to gypsy sequences in one chromosome can repress enhancer promoter interactions in the paired gene located In the other homolog. Proc Natl Acad Sci USA 92: 5184–5188.

    Article  PubMed  CAS  Google Scholar 

  • Gerasimova TI, Byrd K, Corces VG (2000) A chromatin insulator determines the nuclear localization of DNA. Mol Cell 6: 1025–1035.

    Article  PubMed  CAS  Google Scholar 

  • Gerlitz O, Nellen D, Ottiger M, Basler K (2002) A screen for genes expressed in Drosophila imaginal discs. Int J Dev Biol 46: 173–176.

    PubMed  CAS  Google Scholar 

  • Geyer P (1997) The role of insulator elements in defining domains of gene expression. Curr Opin Genet Dev 7: 242–248.

    Article  PubMed  CAS  Google Scholar 

  • Grimaud C, Nègre N, Cavalli G (2006) From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res 14: 00–00 [refers to CHRO 1069].

    Google Scholar 

  • Halfon MS, Gisselbrecht S, Lu J et al. (2002) New fluorescent protein reporters for use with the Drosophila Gal4 expression system and for vital detection of balancer chromosomes. Genesis 34: 135–138.

    Article  PubMed  CAS  Google Scholar 

  • Hartl D, Nurminsky D, Jones R, Lozovskaya E (1994) Genome structure and evolution in Drosophila: applications of the framework P1 map. Proc Natl Acad Sci USA 91: 6824–6829.

    Article  PubMed  CAS  Google Scholar 

  • Hediger F, Taddei A, Neumann FR, Gasser SM (2004) Methods for visualizing chromatin dynamics in living yeast. Methods Enzymol 375: 345–365.

    Article  PubMed  CAS  Google Scholar 

  • Heun P, Laroche T, Raghuraman MK, Gasser SM (2001a) The positioning and dynamics of origins of replication in the budding yeast nucleus. J Cell Biol 152: 385–400.

    Article  PubMed  CAS  Google Scholar 

  • Heun P, Laroche T, Shimada K et al. (2001b) Chromosome dynamics in the yeast interphase nucleus. Science 294: 2181–2186.

    Article  PubMed  CAS  Google Scholar 

  • Houtsmuller AB, Vermeulen W (2001) Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem Cell Biol 115: 13–21.

    PubMed  CAS  Google Scholar 

  • Kellogg DR, Mitchison TJ, Alberts BM (1988) Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103: 675–686.

    PubMed  CAS  Google Scholar 

  • Kimura H (2005) Histone dynamics in living cells revealed by photobleaching. DNA Repair (Amst) 4: 939–950.

    Article  CAS  Google Scholar 

  • Kosman D, Small S, Reinitz J (1998) Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208: 290–294.

    Article  PubMed  CAS  Google Scholar 

  • Kosman D, Reinitz J, Sharp D (1999) Automated assay of gene expression at cellular resolution. In Altman R, Dunker K, Hunter L, Klein T, eds., Proceedings of the 1998 Pacific Symposium on Biocomputing, pp. 6–17.

  • Kraut R, Zinn K (2004) Roundabout 2 regulates migration of sensory neurons by signaling in trans. Curr Biol 14: 1319–1329.

    Article  PubMed  CAS  Google Scholar 

  • Levi V, Ruan Q, Plutz M et al. (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys J 89: 4275–4285.

    Article  PubMed  CAS  Google Scholar 

  • Lifton R, Goldberg M, Karp R, Hogness D (1978) The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. CSH Symp Quant Biol 42: 1047–1051.

    CAS  Google Scholar 

  • Lippincott-Schwartz J, Patterson GH (2003) Development and use of fluorescent protein markers in living cells. Science 300: 87–91.

    Article  PubMed  CAS  Google Scholar 

  • Luschnig S, Moussian B, Krauss J et al. (2004) An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics 167: 325–342.

    Article  PubMed  CAS  Google Scholar 

  • Marshall WF, Straight A, Marko JF et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7: 930–939.

    Article  PubMed  CAS  Google Scholar 

  • Minden JS, Agard DA, Sedat JW, Alberts BM (1989) Direct cell lineage analysis in Drosophila melanogaster by time-lapse, three-dimensional optical microscopy of living embryos. J Cell Biol 109: 505–516.

    Article  PubMed  CAS  Google Scholar 

  • Miyawaki A (2006) New fluorescent probes and new perspective in bioscience. SPIE 6089: 18.

    Google Scholar 

  • Murray MJ, Merritt DJ, Brand AH, Whitington PM (1998) In vivo dynamics of axon pathfinding in the Drosophila CNS: a time-lapse study of an identified motorneuron. J Neurobiol 37: 607–621.

    Article  PubMed  CAS  Google Scholar 

  • Painter T (1934) Salivary chromosomes and the attack on the gene. J Hered 25: 465–476.

    Google Scholar 

  • Phair RD, Misteli T (2001) Kinetic modelling approaches to in vivo imaging. Nature Rev Mol Cell Biol 2: 898–907.

    Article  CAS  Google Scholar 

  • Post JN, Lidke KA, Rieger B, Arndt-Jovin DJ (2005) One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos. FEBS Lett 579: 325–330.

    Article  PubMed  CAS  Google Scholar 

  • Robinett CC, Straight A, Li G et al. (1996) In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J Cell Biol 135: 1685–1700.

    Article  PubMed  CAS  Google Scholar 

  • Saint R, Clarkson M (2000) Pictures in cell biology. A functional marker for Drosophila chromosomes in vivo. Trends Cell Biol 10: 553.

    Article  PubMed  CAS  Google Scholar 

  • Schmid A, Chiba A, Doe CQ (1999) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126: 4653–4689.

    PubMed  CAS  Google Scholar 

  • Shao Z, Raible F, Mollaaghababa R et al. (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37–46.

    Article  PubMed  CAS  Google Scholar 

  • Sigrist CJ, Pirrotta V (1997) Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes. Genetics 147: 209–221.

    PubMed  CAS  Google Scholar 

  • Spradling A, Penman S, Pardue ML (1975) Analysis of Drosophila messenger RNA by in-situ hybridization sequences transcribed in normal and heat shocked cultured cells. Cell 4: 395–404.

    Article  PubMed  CAS  Google Scholar 

  • Sprague BL, Pego RL, Stavreva DA, McNally JG (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J 86: 3473–3495.

    Article  PubMed  CAS  Google Scholar 

  • Straight AF, Belmont AS, Robinett CC, Murray AW (1996) GFP tagging of budding yeast chromosomes reveals that protein–protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599–1608.

    Article  PubMed  CAS  Google Scholar 

  • Thakar R, Csink AK (2005) Changing chromatin dynamics and nuclear organization during differentiation in Drosophila larval tissue. J Cell Sci 118: 951–960.

    Article  PubMed  CAS  Google Scholar 

  • Tumbar T, Sudlow G, Belmont AS (1999) Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J Cell Biol 145: 1341–1354.

    Article  PubMed  CAS  Google Scholar 

  • Vazquez J, Belmont AS, Sedat JW (2001) Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus. Curr Biol 11: 1227–1239.

    Article  PubMed  CAS  Google Scholar 

  • Volpi EV, Chevret E, Jones T et al. (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113: 1565–1576.

    PubMed  CAS  Google Scholar 

  • Wensink PC, Finnegan D, Donelson J, Hogness D (1974) A system for mapping DNA sequences in the chromosomes of Drosophila melanogaster. Cell 3: 315–325.

    Article  PubMed  CAS  Google Scholar 

  • White J, Stelzer E (1999) Photobleaching GFP reveals protein dynamics inside live cells. Trends Cell Biol 9: 61–65.

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Rubin GM (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223–1237.

    PubMed  CAS  Google Scholar 

  • Yeh E, Gustafson K, Boulianne GL (1995) Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc Natl Acad Sci USA 92: 7036–7040.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. G. Ficz for providing the images of Pc-GFP and Ph-GFP expression in Drosophila embryos and larval tissues as well as for the FRAP curves presented here. We thank both Dr. Ficz and Dr. J. Post for helpful discussions.

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, 37070, Göttingen, Germany

    Cornelia Fritsch, Ginette Ploeger & Donna J. Arndt-Jovin

  2. Molecular Cytology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands

    Ginette Ploeger

Authors
  1. Cornelia Fritsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ginette Ploeger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donna J. Arndt-Jovin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donna J. Arndt-Jovin.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fritsch, C., Ploeger, G. & Arndt-Jovin, D.J. Drosophila under the lens: imaging from chromosomes to whole embryos. Chromosome Res 14, 451–464 (2006). https://doi.org/10.1007/s10577-006-1068-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1068-z

Key words

Search

Navigation