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Drosophila melanogaster as a Model of Developmental Genetics: Modern Approaches and Prospects

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Abstract

For more than a 100 years, the fruit fly Drosophila melanogaster has successfully served as a universal model in various genetic studies, including studies into the genetic control of individual development. To date, a whole arsenal of reverse genetics methods has been developed for Drosophila, making it quite easy to manipulate its genome, which allows Drosophila to be considered one of the most powerful models of developmental genetics. The review considers the main modern methods for studying the expression and function of genes in Drosophila and the prospects for their use.

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REFERENCES

  1. Ameres, S.L. and Zamore, P.D., Diversifying microRNA sequence and function, Nat. Rev. Mol. Cell Biol., 2013, vol. 14, no. 8, pp. 475–488.

    CAS  PubMed  Google Scholar 

  2. Amourda, C. and Saunders, T.E., Gene expression boundary scaling and organ size regulation in the Drosophila embryo, Dev. Growth Differ, 2017, vol. 59, no. 1, pp. 21–32.

    PubMed  Google Scholar 

  3. Bageritz, J., Willnow, P., Valentini, E., et al., Gene expression atlas of a developing tissue by single cell expression correlation analysis, Nat. Methods, 2019, vol. 16, no. 8, pp. 750–756.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Banerjee, U., Girard, J.R., Goins, L.M., et al., Drosophila as a genetic model for hematopoiesis, Genetics, 2019, vol. 211, no. 2, pp. 367–417.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Bateman, J.R., Lee, A.M., and Wu, C.T., Site-specific transformation of Drosophila via PhiC31 integrase-mediated cassette exchange, Genetics, 2006, vol. 173, pp. 769–777.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bellen, H.J., Levis, R.W., Liao, G., et al., The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes, Genetics, 2004, vol. 167, no. 2, pp. 761–781.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Bischof, J., Maeda, R.K., Hediger, M., et al., An optimized transgenesis system for Drosophila using germ-line-specific PhiC31integrases, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, pp. 3312–3317.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bosch, J.A., Sumabat, T.M., and Hariharan, I.K., Persistence of RNAi-mediated knockdown in Drosophila complicates mosaic analysis yet enables highly sensitive lineage tracing, Genetics, 2016, vol. 203, no. 1, pp. 109–118.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Brand, A.H. and Perrimon, N., Targeted gene expression as a means of altering cell fates and generating dominant phenotypes, Development, 1993, vol. 118, no. 2, pp. 401–415.

    CAS  PubMed  Google Scholar 

  10. Branda, C.S. and Dymecki, S.M., Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice, Dev. Cell, 2004, vol. 6, no. 1, pp. 7–28.

    CAS  PubMed  Google Scholar 

  11. Chandran, R.R., Iordanou, E., Ajja, C., et al., Gene expression profiling of Drosophila tracheal fusion cells, Gene Expr. Patterns, 2014, vol. 15, no. 2, pp. 112–123.

    CAS  PubMed  Google Scholar 

  12. Dietzl, G., Chen, D., Schnorrer, F., et al., A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila,Nature, 2007, vol. 448, no. 7150, pp. 151–156.

    CAS  PubMed  Google Scholar 

  13. Duc, C., Yoth, M., Jensen, S., et al., Trapping a somatic endogenous retrovirus into a germline pirna cluster immunizes the germline against further invasion, Genome Biol., 2019, vol. 20, no. 1, p. 127.

    PubMed  PubMed Central  Google Scholar 

  14. Ewen-Campen, B., Yang-Zhou, D., Fernandes, V.R., et al., Optimized strategy for in vivo cas9-activation in Drosophila, Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, pp. 9409–9414.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Fernandez, C. and Lagha, M., Lighting up gene activation in living Drosophila embryos, Methods Mol. Biol., 2019, vol. 2038, pp. 63–74.

    CAS  PubMed  Google Scholar 

  16. Frasch, M., Genome-wide approaches to Drosophila heart development, J. Cardiovasc. Dev. Dis., 2016, vol. 3, no. 2. pii:20.

    PubMed  PubMed Central  Google Scholar 

  17. Frickenhaus, M., Wagner, M., Mallik, M., et al., Highly efficient cell-type-specific gene inactivation reveals a key function for the Drosophila FUS homolog cabeza in neurons, Sci. Rep., 2015, vol. 5, p. 9107.

    PubMed  PubMed Central  Google Scholar 

  18. Gaziova, I., Bonnette, P.C., Henrich, V.C., and Jindra, M., Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis, Development, 2004, vol. 131, no. 11, pp. 2715–2725.

    CAS  PubMed  Google Scholar 

  19. Golic, K.G. and Golic, M.M., Engineering the Drosophila genome: chromosome rearrangements by design, Genetics, 1996, vol. 144, pp. 1693–1711.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Groth, A.C., Fish, M., Nusse, R., et al., Construction of transgenic Drosophila by using the site-specific integrase from phage PhiC31, Genetics, 2004, vol. 166, pp. 1775–1782.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Gunage, R.D., Dhanyasi, N., Reichert, H., et al., Drosophila adult muscle development and regeneration, Semin. Cell Dev. Biol., 2017, vol. 72, pp. 56–66.

    CAS  PubMed  Google Scholar 

  22. Hsu, H.J., Bahader, M., and Lai, C.M., Molecular control of the female germline stem cell niche size in Drosophila,Cell Mol. Life Sci., 2019, vol. 76, no. 21, pp. 4309–4317.

    CAS  PubMed  Google Scholar 

  23. Hudson, A.M. and Cooley, L., Methods for studying oogenesis, Methods, 2014, vol. 68, no. 1, pp. 207–217.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Jennett, A., Rubin, G., Ngo, T., et al., A GAL4-driver line resource for Drosophila neurobiology, Cell Rep., 2012, vol. 2, no. 4, pp. 991–1001.

    Google Scholar 

  25. Jin, M., Eblimit, A., Pulikkathara, M., et al., Conditional knockout of retinal determination genes in differentiating cells in Drosophila,FEBS J., 2016, vol. 283, no. 15, pp. 2754–2766.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Kane, N.S., Vora, M., Varre, K.J., et al., Efficient screening of crispr/cas9-induced events in Drosophila using a co-CRISPR strategy, G3 Genes Genomes Genet., 2017, vol. 7, pp. 87–93.

  27. Kennerdell, J.R. and Carthew, R.W., Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway, Cell, 1998, vol. 95, no. 7, pp. 1017–1026.

    CAS  PubMed  Google Scholar 

  28. Kidwell, M.G., Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation, Genetics, 1985, vol. 111, pp. 337–350.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Knapp, J.M., Chung, P., and Simpson, J.H., Generating customized transgene landing sites and multi-transgene arrays in Drosophila using PhiC31 integrase, Genetics, 2015, vol. 199, pp. 919–934.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kondo, S. and Ueda, R., Highly improved gene targeting by germline-specific Cas9 expression in Drosophila,Genetics, 2013, vol. 195, pp. 715–721.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Kopke, D.L., Leahy, S.N., Vita, D.J., et al., Carrier of wingless (cow) regulation of Drosophila neuromuscular junction development, eNeuro, 2020. pii: ENEURO.0285-19.2020.

  32. Lee, T. and Luo, L., Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development, Trends Neurosci., 2001, vol. 24, no. 5, pp. 251–254.

    CAS  PubMed  Google Scholar 

  33. Liu, Z., Chen, Y., and Rao, Y., An RNAi screen for secreted factors and cell-surface players in coordinating neuron and glia development in Drosophila,Mol. Brain, 2020, vol. 13, no. 1, p. 1.

    PubMed  PubMed Central  Google Scholar 

  34. Lobo, N., Li, X., and Fraser, M.J., Transposition of the piggybac element in embryos of Drosophila melanogaster, Aedes aegypti and Trichoplusia ni,Mol. Gen. Genet., 1999, vol. 261, pp. 803–810.

    CAS  PubMed  Google Scholar 

  35. Lott, S.E., Villalta, J.E., Schroth, G.P., et al., Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq, PLoS Biol., 2011, vol. 9, no. 2. e1000590.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Loukeris, T.G., Arca, B., Livadaras, I., et al., Introduction of the transposable element minos into the germ line of Drosophila melanogaster,Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, pp. 9485–9489.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Mazina, M.Y., Krasnov, A.N., Georgiev, P.G., et al., The development of reporter system for the investigation of molecular mechanisms of ecdysone response, Dokl. Biochem. Biophys., 2019, vol. 485, no. 1, pp. 138–140.

    CAS  PubMed  Google Scholar 

  38. McGuire, S.E., Roman, G., and Davis, R.L., Gene expression systems in Drosophila: a synthesis of time and space, Trends Genet., 2004, vol. 20, no. 8, pp. 384–391.

    CAS  PubMed  Google Scholar 

  39. Nagarkar-Jaiswal, S., DeLuca, S.Z., Lee, P.-T., et al., A genetic toolkit for tagging intronic MiMIC containing genes, Elife, 2015, vol. 4. e08469.

    PubMed Central  Google Scholar 

  40. Nakazawa, N., Taniguchi, K., Okumura, T., et al., A novel cre/loxp system for mosaic gene expression in the Drosophila embryo, Dev. Dyn., 2012, vol. 241, pp. 965–974.

    CAS  PubMed  Google Scholar 

  41. Neumüller, R.A., Wirtz-Peitz, F., Lee, S., et al., Stringent analysis of gene function and protein-protein interactions using fluorescently tagged genes, Genetics, 2012, vol. 190, no. 3, pp. 931–940.

    PubMed  PubMed Central  Google Scholar 

  42. Perkins, L.A., Holderbaum, L., Tao, R., et al., The transgenic RNAi Project at Harvard Medical School: resources and validation, Genetics, 2015, vol. 201, no. 3, pp. 843–852.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Port, F., Chen, H.M., Lee, T., et al., Optimized CRISPR/ Cas tools for efficient germline and somatic genome engineering in Drosophila,Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, pp. E2967–E2976.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Ramadan, N., Flockhart, I., Booker, M., et al., Design and implementation of high-throughput RNAi screens in cultured Drosophila cells, Nat. Protoc., 2007, vol. 2, no. 9, pp. 2245–2264.

    CAS  PubMed  Google Scholar 

  45. Riggleman, B., Wieschaus, E., and Schedl, P., Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene, Genes Dev., 1989, vol. 3, pp. 96–113.

    CAS  PubMed  Google Scholar 

  46. Rodal, A.A., Del Signore, S.J., and Martin, A.C., Drosophila comes of age as a model system for understanding the function of cytoskeletal proteins in cells, tissues, and organisms, Cytoskeleton (Hoboken), 2015, vol. 72, no. 5, pp. 207–224.

    CAS  PubMed  Google Scholar 

  47. Rong, Y.S., Gene targeting by homologous recombination: a powerful addition to the genetic arsenal for Drosophila geneticists, Biochem. Biophys. Res. Commun., 2002, vol. 297, no. 1, pp. 1–5.

    CAS  PubMed  Google Scholar 

  48. Rubin, T. and Huynh, J.R., Mosaic analysis in the Drosophila melanogaster ovary, Methods Mol. Biol., 2015, vol. 1328, pp. 29–55.

    CAS  PubMed  Google Scholar 

  49. Rubin, G.M. and Spradling, A.C., Genetic transformation of Drosophila with transposable element vectors, Science, 1982, vol. 218, pp. 348–353.

    CAS  PubMed  Google Scholar 

  50. Ryder, E. and Russell, S., Transposable elements as tools for genomics and genetics in Drosophila,Brief Funct. Genomic Proteomic, 2003, vol. 2, no. 1, pp. 57–71.

    CAS  PubMed  Google Scholar 

  51. Ryder, E., Ashburner, M., Bautista-Llacer, R., et al., The DrosDel deletion collection: a Drosophila genome-wide chromosomal deficiency resource, Genetics, 2007, vol. 177, pp. 615–629.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Schertel, C., Albacara, M., Rockel-Bauer, C., et al., A large-scale, in vivo transcription factor screen defines bivalent chromatin as a key property of regulatory factors mediating Drosophila wing development, Genome Res., 2015, vol. 25, no. 4, pp. 514–523.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Spirov, A.V. and Myasnikova, E.M., Evolutionary stability of gene regulatory networks that define the temporal identity of neuroblasts, Mol. Biol. (Moscow), 2019, vol. 53, no. 2, pp. 225–239.

    CAS  Google Scholar 

  54. Theodosiou, N.A. and Xu, T., Use of FLP/FRT system to study Drosophila development, Methods, 1998, vol. 14, no. 4, pp. 355–365.

    CAS  PubMed  Google Scholar 

  55. Thorn, K., Genetically encoded fluorescent tags, Mol. Biol. Cell, 2017, vol. 28, pp. 848–857.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Venken, K.J., Schulze, K.L., Haelterman, N.A., et al., Mimic: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes, Nat. Methods, 2011, vol. 8, pp. 737–743.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Weisman, N.Ya., Genetic and epigenetic pathways of lethal (2) giant larvae Tumor Suppressor in Drosophila melanogaster,Russ. J. Genet., 2019, vol. 55, no. 2, pp. 133–143.

    CAS  Google Scholar 

  58. Xu, X.S., Gantz, V.M., Siomava, N., et al., CRISPR/Cas9 and active genetics-based trans-species replacement of the endogenous Drosophila kni-L2 CRM reveals unexpected complexity, Elife, 2017, vol. 6. pii:e30281.

    PubMed  PubMed Central  Google Scholar 

  59. Xue, Z., Ren, M., Wu, M., et al., Efficient gene knock-out and knock-in with transgenic Cas9 in Drosophila,G3 (Bethesda), 2014, vol. 4, no. 5, pp. 925–929.

    CAS  PubMed  Google Scholar 

  60. Yang, C.P., Fu, C.C., Sugino, K., et al., Transcriptomes of lineage-specific Drosophila neuroblasts profiled by genetic targeting and robotic sorting, Development, 2016, vol. 143, no. 3, pp. 411–421.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhou, J., Schor, I.E., Yao, V., et al., Accurate genome-wide predictions of spatio-temporal gene expression during embryonic development, PLoS Genet., 2019, vol. 15, no. 9. e1008382.

    CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

I thank Dr. Sci. (Biol.) O.B. Simonova for fruitful discussion of the article.

Funding

The work was carried out as part of the Molecular Genetic Mechanisms of Genome Instability and Mutagenesis in Animals and Humans program of the Faculty of Biology of Moscow State University (AAAA-A16-116021660038-4).

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Correspondence to L. N. Nefedova.

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This article does not contain any studies performed by the author with the participation of people or the use of animals as objects.

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Translated by N. Smolina

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Nefedova, L.N. Drosophila melanogaster as a Model of Developmental Genetics: Modern Approaches and Prospects. Russ J Dev Biol 51, 201–211 (2020). https://doi.org/10.1134/S1062360420040050

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