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Drosophila melanogaster Oogenesis: An Overview

  • John M. McLaughlin
  • Diana P. BratuEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1328)

Abstract

The Drosophila melanogaster ovary has served as a popular and successful model for understanding a wide range of biological processes: stem cell function, germ cell development, meiosis, cell migration, morphogenesis, cell death, intercellular signaling, mRNA localization, and translational control. This review provides a brief introduction to Drosophila oogenesis, along with a survey of its diverse biological topics and the advanced genetic tools that continue to make this a popular developmental model system.

Keywords

Flp-FRT Patterning Follicle cells Morphogenesis Germ plasm Mosaics P element RNAi Drosophila Oogenesis Oocyte mRNA localization Gal4 Live Imaging CRISPR Fluorescence 

Notes

Acknowledgements

We thank Emily Hudson for assistance with the art included in the figures, and members of the Bratu laboratory for helpful comments on the manuscript. JMM and DPB were supported by an NSF CAREER Award to DPB.

References

  1. 1.
    Roote J, Prokop A (2013) How to design a genetic mating scheme: a basic training package for Drosophila genetics. G3 (Bethesda) 3:353–358CrossRefGoogle Scholar
  2. 2.
    Telfer WH (1975) Development and physiology of the oocyte-nurse cell syncytium. Adv Insect Physiol 11:223–319CrossRefGoogle Scholar
  3. 3.
    Tworzydlo W, Bilinski SM, Kocarek P et al (2010) Ovaries and germline cysts and their evolution in Dermaptera (Insecta). Arthropod Struct Dev 39:360–368PubMedCrossRefGoogle Scholar
  4. 4.
    Swevers L, Raikhel AS, Sappington TW et al (2005) Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. In: Gilbert L (ed) Comprehensive molecular insect science, vol 1. Elsevier BV, Oxford, pp 87–155CrossRefGoogle Scholar
  5. 5.
    Godt D, Laski FA (1995) Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric à brac. Development 121:173–187PubMedGoogle Scholar
  6. 6.
    Voog J, Jones DL (2010) Stem cells and the niche: a dynamic duo. Cell Stem Cell 6:103–115PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Lopez-Onieva L, Fernandez-Minan A, Gonzalez-Reyes A (2008) Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary. Development 135:533–540PubMedCrossRefGoogle Scholar
  8. 8.
    Forbes AJ, Lin H, Ingham PW et al (1996) hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122:1125–1135PubMedGoogle Scholar
  9. 9.
    Spradling A, Fuller MT, Braun RE et al (2011) Germline stem cells. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a002642 PubMedCentralPubMedGoogle Scholar
  10. 10.
    Losick VP, Morris LX, Fox DT et al (2011) Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell 21:159–171PubMedCrossRefGoogle Scholar
  11. 11.
    King RC (1970) Ovarian development in Drosophila melanogaster. Academic, New YorkGoogle Scholar
  12. 12.
    Kirilly D, Wang S, Xie T (2011) Self-maintained escort cells form a germline stem cell differentiation niche. Development 138:5087–5097PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Decotto E, Spradling AC (2005) The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell 9:501–510PubMedCrossRefGoogle Scholar
  14. 14.
    Xie T (2012) Control of germline stem cell self-renewal and differentiation in the Drosophila ovary: concerted actions of niche signals and intrinsic factors. Wiley Interdiscip Rev Dev Biol 2:261–273PubMedGoogle Scholar
  15. 15.
    Morris LX, Spradling AC (2011) Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138:2207–2215PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    King RC, Aggarwal SK, Aggarwal U (1968) The development of the Drosophila female reproductive system. J Morphol 124:142–166CrossRefGoogle Scholar
  17. 17.
    Roth S, Lynch JA (2009) Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a001891 PubMedCentralPubMedGoogle Scholar
  18. 18.
    Huynh JR (2005) Fusome as a cell-cell communication channel of Drosophila ovarian cyst. In: Baluska F, Volkmann D, Barlow PW (eds) Cell-cell channels. Eurekah Bioscience, Georgetown, TX, pp 1–19Google Scholar
  19. 19.
    Warn RM, Gutzeit HO, Smith L et al (1985) F-actin rings are associated with the ring canals of the Drosophila egg chamber. Exp Cell Res 157:355–363PubMedCrossRefGoogle Scholar
  20. 20.
    Field CM, Alberts BM (1995) Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131:165–178PubMedCrossRefGoogle Scholar
  21. 21.
    Robinson DN, Cant K, Cooley L (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120:2015–2025PubMedGoogle Scholar
  22. 22.
    Huynh JR, St Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14:R438–R449PubMedCrossRefGoogle Scholar
  23. 23.
    Keyes LN, Spradling AC (1997) The Drosophila gene fs(2)cup interacts with otu to define a cytoplasmic pathway required for the structure and function of germ-line chromosomes. Development 124:1419–1431PubMedGoogle Scholar
  24. 24.
    Lantz V, Chang JS, Horabin JI et al (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8:598–613PubMedCrossRefGoogle Scholar
  25. 25.
    Suter B, Romberg LM, Steward R (1989) Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains. Genes Dev 3:1957–1968PubMedCrossRefGoogle Scholar
  26. 26.
    de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125:2781–2789PubMedGoogle Scholar
  27. 27.
    Riechmann V, Ephrussi A (2001) Axis formation during Drosophila oogenesis. Curr Opin Genet Dev 11:374–383PubMedCrossRefGoogle Scholar
  28. 28.
    Nystul T, Spradling A (2007) An epithelial niche in the Drosophila ovary undergoes long-range stem cell replacement. Cell Stem Cell 1:277–285PubMedCrossRefGoogle Scholar
  29. 29.
    Sahai-Hernandez P, Nystul TG (2013) A dynamic population of stromal cells contributes to the follicle stem cell niche in the Drosophila ovary. Development 140:4490–4498PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Song X, Xie T (2003) wingless signaling regulates the maintenance of ovarian somatic stem cells in Drosophila. Development 130:3259–3268PubMedCrossRefGoogle Scholar
  31. 31.
    Kirilly D, Spana EP, Perrimon N et al (2005) BMP signaling is required for controlling somatic stem cell self-renewal in the Drosophila ovary. Dev Cell 9:651–662PubMedCrossRefGoogle Scholar
  32. 32.
    Bolivar J, Pearson J, Lopez-Onieva L et al (2006) Genetic dissection of a stem cell niche: the case of the Drosophila ovary. Dev Dyn 235:2969–2979PubMedCrossRefGoogle Scholar
  33. 33.
    Wu X, Tanwar PS, Raftery LA (2008) Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19:271–282PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Tworoger M, Larkin MK, Bryant Z et al (1999) Mosaic analysis in the Drosophila ovary reveals a common hedgehog-inducible precursor stage for stalk and polar cells. Genetics 151:739–748PubMedCentralPubMedGoogle Scholar
  35. 35.
    Roth S, Neuman-Silberberg FS, Barcelo G et al (1995) cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81:967–978PubMedCrossRefGoogle Scholar
  36. 36.
    Bai J, Montell D (2002) Eyes absent, a key repressor of polar cell fate during Drosophila oogenesis. Development 129:5377–5388PubMedCrossRefGoogle Scholar
  37. 37.
    St Johnston D, Gonzalez-Reyes A (1998) Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis. Development 125:2837–2846PubMedGoogle Scholar
  38. 38.
    Deng WM, Althauser C, Ruohola-Baker H (2001) Notch-Delta signaling induces a transition from mitotic cell cycle to endocycle in Drosophila follicle cells. Development 128:4737–4746PubMedGoogle Scholar
  39. 39.
    Yoon WH, Meinhardt H, Montell DJ (2011) miRNA-mediated feedback inhibition of JAK/STAT morphogen signalling establishes a cell fate threshold. Nat Cell Biol 13:1062–1069PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    He L, Wang X, Montell DJ (2011) Shining light on Drosophila oogenesis: live imaging of egg development. Curr Opin Genet Dev 21:612–619PubMedCrossRefGoogle Scholar
  41. 41.
    Prasad M, Wang X, He L et al (2011) Border cell migration: a model system for live imaging and genetic analysis of collective cell movement. Methods Mol Biol 769:277–286PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Dobens L, Raftery LA (2008) Integration of epithelial patterning and morphogenesis in Drosophila ovarian follicle cells. Dev Dyn 218:80–93CrossRefGoogle Scholar
  43. 43.
    Grammont M (2007) Adherens junction remodeling by the Notch pathway in Drosophila melanogaster oogenesis. J Cell Biol 177:139–150PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331:1071–1074PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Bilder D, Haigo SL (2012) Expanding the morphogenetic repertoire: perspectives from the Drosophila egg. Dev Cell 22:12–23PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Gates J (2012) Drosophila egg chamber elongation: insights into how tissues and organs are shaped. Fly 6:213–227PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Claycomb JM, Orr-Weaver TL (2005) Developmental gene amplification: insights into DNA replication and gene expression. Trends Genet 21:149–162PubMedCrossRefGoogle Scholar
  48. 48.
    Royzman I, Orr-Weaver TL (1998) S phase and differential DNA replication during Drosophila oogenesis. Genes Cells 3:767–776PubMedCrossRefGoogle Scholar
  49. 49.
    Dej KJ, Spradling AC (1999) The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis. Development 126:293–303PubMedGoogle Scholar
  50. 50.
    Nordman J, Orr-Weaver TL (2012) Regulation of DNA replication during development. Development 139:455–464PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Klusza S, Deng WM (2011) At the crossroads of differentiation and proliferation: precise control of cell-cycle changes by multiple signaling pathways in Drosophila follicle cells. Bioessays 33:124–134PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Kronja I, Orr-Weaver TL (2011) Translational regulation of the cell cycle: when, where, how and why? Philos Trans R Soc Lond B Biol Sci 366:3638–3652PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Von Stetina JR, Orr-Weaver TL (2011) Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a005553 Google Scholar
  54. 54.
    Bosco G, Orr-Weaver TL (2002) The cell cycle during oogenesis and early embryogenesis in Drosophila. Adv Dev Biol Biochem. doi: 10.1016/S1569-1799(02)12026-0 Google Scholar
  55. 55.
    Smith PA, King RC (1968) Genetic control of synaptonemal complexes in Drosophila melanogaster. Genetics 60:335–351PubMedCentralPubMedGoogle Scholar
  56. 56.
    Mahowald AP, Goralski TJ, Caulton JH (1983) In vitro activation of Drosophila eggs. Dev Biol 98:437–445PubMedCrossRefGoogle Scholar
  57. 57.
    Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801PubMedCrossRefGoogle Scholar
  58. 58.
    Ephrussi A, Dickinson LK, Lehmann R (1991) oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50PubMedCrossRefGoogle Scholar
  59. 59.
    Kim-Ha J, Smith JL, Macdonald PM (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35PubMedCrossRefGoogle Scholar
  60. 60.
    St Johnston D, Beuchle D, Nusslein-Volhard C (1991) staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66:51–63PubMedCrossRefGoogle Scholar
  61. 61.
    Kugler JM, Lasko P (2009) Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly 3:15–28PubMedCrossRefGoogle Scholar
  62. 62.
    Lasko P (2011) Posttranscriptional regulation in Drosophila oocytes and early embryos. Wiley Interdiscip Rev RNA 2:408–416PubMedCrossRefGoogle Scholar
  63. 63.
    Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136:719–730PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Cooperstock RL, Lipshitz HD (2001) RNA localization and translational regulation during axis specification in the Drosophila oocyte. Int Rev Cytol 203:541–566PubMedCrossRefGoogle Scholar
  65. 65.
    Becalska AN, Gavis ER (2009) Lighting up mRNA localization in Drosophila oogenesis. Development 136:2493–2503PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Chekulaeva M, Hentze MW, Ephrussi A (2006) Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell 124:521–533PubMedCrossRefGoogle Scholar
  67. 67.
    Vardy L, Orr-Weaver TL (2007) Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol 17:547–554PubMedCrossRefGoogle Scholar
  68. 68.
    Bratu DP, Cha BJ, Mhlanga MM et al (2003) Visualizing the distribution and transport of mRNAs in living cells. Proc Natl Acad Sci U S A 100:13308–13313PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Mhlanga MM, Bratu DP, Genovesio A et al (2009) In vivo colocalisation of oskar mRNA and trans-acting proteins revealed by quantitative imaging of the Drosophila oocyte. PLoS One. doi: 10.1371/journal.pone.0006241 PubMedCentralPubMedGoogle Scholar
  70. 70.
    Zimyanin VL, Belaya K, Pecreaux J et al (2008) In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134:843–853PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Parton RM, Hamilton RS, Ball G et al (2011) A PAR-1-dependent orientation gradient of dynamic microtubules directs posterior cargo transport in the Drosophila oocyte. J Cell Biol 194:121–135PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Sinsimer KS, Lee JJ, Thiberge SY et al (2013) Germ plasm anchoring is a dynamic state that requires persistent trafficking. Cell Rep 5:1169–1177PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Cha BJ, Koppetsch BS, Theurkauf WE (2001) In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106:35–46PubMedCrossRefGoogle Scholar
  74. 74.
    Ewen-Campen B, Donoughe S, Clarke DN et al (2013) Germ cell specification requires zygotic mechanisms rather than germ plasm in a basally branching insect. Curr Biol 23:835–842PubMedCrossRefGoogle Scholar
  75. 75.
    Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884PubMedCrossRefGoogle Scholar
  76. 76.
    Hegner RW (1908) Effects of removing the germ-cell determinants from the eggs of some chrysomelid beetles. Preliminary report. Biol Bull 16:19–26CrossRefGoogle Scholar
  77. 77.
    Kloc M, Bilinksi S, Etkin LD (2004) The balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59:1–36PubMedCrossRefGoogle Scholar
  78. 78.
    Mahowald AP (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203:187–213PubMedCrossRefGoogle Scholar
  79. 79.
    Kobayashi S, Amikura R, Okada M (1994) Localization of mitochondrial large rRNA in germinal granules and the consequent segregation of germ line. Int J Dev Biol 38:193–199PubMedGoogle Scholar
  80. 80.
    Arkov AL, Ramos A (2010) Building RNA-protein granules: insight from the germline. Trends Cell Biol 20:482–490PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Kirino Y, Vourekas A, Sayed N et al (2010) Arginine methylation of Aubergine mediates Tudor binding and germ plasm localization. RNA 16:70–78PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387–392PubMedCrossRefGoogle Scholar
  83. 83.
    Rongo C, Lehmann R (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet 12:102–109PubMedCrossRefGoogle Scholar
  84. 84.
    Starz-Gaiano M, Lehmann R (2001) Moving towards the next generation. Mech Dev 105:5–18PubMedCrossRefGoogle Scholar
  85. 85.
    Markussen FH, Michon AM, Breitwieser W et al (1995) Translational control of oskar generates Short OSK, the isoform that induces pole plasm assembly. Development 121:3723–3732PubMedGoogle Scholar
  86. 86.
    Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55:1141–1163PubMedCrossRefGoogle Scholar
  87. 87.
    Vanzo NF, Ephrussi A (2002) Oskar anchoring restricts pole plasm to the posterior of the Drosophila oocyte. Development 129:3705–3714PubMedGoogle Scholar
  88. 88.
    Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci U S A 71:1016–1020PubMedCentralPubMedCrossRefGoogle Scholar
  89. 89.
    St Johnston D (2002) The art and design of genetic screens: Drosophila melanogaster. Nat Rev Genet 3:176–188PubMedCrossRefGoogle Scholar
  90. 90.
    Venken KJ, Bellen HJ (2014) Chemical mutagens, transposons, and transgenes to interrogate gene function in Drosophila melanogaster. Methods 68:15–28PubMedCentralPubMedCrossRefGoogle Scholar
  91. 91.
    Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347PubMedCrossRefGoogle Scholar
  92. 92.
    Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353PubMedCrossRefGoogle Scholar
  93. 93.
    Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415PubMedGoogle Scholar
  94. 94.
    Duffy JB (2002) GAL4 system in Drosophila: A fly geneticist’s Swiss army knife. Genesis 34:1–15PubMedCrossRefGoogle Scholar
  95. 95.
    Jory A, Estella C, Giorgianni MW et al (2012) A survey of 6,300 genomic fragments for cis-regulatory activity in the imaginal discs of Drosophila melanogaster. Cell Rep 2:1014–1024PubMedCentralPubMedCrossRefGoogle Scholar
  96. 96.
    Manning L, Heckscher ES, Purice MD et al (2012) A resource for manipulating gene expression and analyzing cis-regulatory modules in the Drosophila CNS. Cell Rep 2:1002–1013PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Pfeiffer BD, Jenett A, Hammonds AS et al (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105:9715–9720PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Jenett A, Rubin GM, Ngo TT et al (2012) A GAL4-Driver line resource for Drosophila neurobiology. Cell Rep 2:991–1001PubMedCentralPubMedCrossRefGoogle Scholar
  99. 99.
    Bloomington Drosophila Stock Center. http://flystocks.bio.indiana.edu
  100. 100.
    Vienna Drosophila RNAi Center (VDRC). http://stockcenter.vdrc.at/control/main
  101. 101.
    Kyoto Drosophila Genetic Resource Center (DGRC). https://kyotofly.kit.jp/cgi-bin/stocks/index.cgi
  102. 102.
    Rørth P (1998) Gal4 in the Drosophila female germline. Mech Dev 78:113–118PubMedCrossRefGoogle Scholar
  103. 103.
    Hudson AM, Cooley L (2014) Methods for studying oogenesis. Methods 68:207–217PubMedCentralPubMedCrossRefGoogle Scholar
  104. 104.
    Drosophila Transgenic RNAi Project (TRiP). http://www.flyrnai.org/TRiP-HOME.html
  105. 105.
    Ni JQ, Markstein M, Binari R et al (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5:49–51PubMedCentralPubMedCrossRefGoogle Scholar
  106. 106.
    Dietzl G, Chen D, Schnorrer F et al (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156PubMedCrossRefGoogle Scholar
  107. 107.
    Czech B, Preall JB, McGinn J et al (2013) A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell 50:749–761PubMedCentralPubMedCrossRefGoogle Scholar
  108. 108.
    Handler D, Meixner K, Pizka M et al (2013) The genetic makeup of the Drosophila piRNA pathway. Mol Cell 50:762–777PubMedCentralPubMedCrossRefGoogle Scholar
  109. 109.
    Preall JB, Czech B, Guzzardo PM et al (2012) shutdown is a component of the Drosophila piRNA biogenesis machinery. RNA 18:1446–1457PubMedCentralPubMedCrossRefGoogle Scholar
  110. 110.
    McConnell KH, Dixon M, Calvi BR (2012) The histone acetyltransferases CBP and Chameau integrate developmental and DNA replication programs in Drosophila ovarian follicle cells. Development 139:3880–3890PubMedCentralPubMedCrossRefGoogle Scholar
  111. 111.
    Geisbrecht ER, Sawant K, Su Y et al (2013) Genetic interaction screens identify a role for Hedgehog signaling in Drosophila border cell migration. Dev Dyn 242:414–431PubMedCentralPubMedCrossRefGoogle Scholar
  112. 112.
    Gu T, Elgin SC (2013) Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet. doi: 10.1371/journal.pgen.1003780 Google Scholar
  113. 113.
    Pfeiffer BD, Ngo TT, Hibbard KL et al (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186:735–755PubMedCentralPubMedCrossRefGoogle Scholar
  114. 114.
    del Valle Rodriguez A, Didiano D, Desplan C (2012) Power tools for gene expression and clonal analysis in Drosophila. Nat Methods 9:47–55CrossRefGoogle Scholar
  115. 115.
    Xu T, Rubin GM (2012) The effort to make mosaic analysis a household tool. Development 139:4501–4503PubMedCentralPubMedCrossRefGoogle Scholar
  116. 116.
    Patterson JT (1929) The production of mutations in somatic cells of Drosophila melanogaster by means of X-rays. J Exp Zool 53:327–372CrossRefGoogle Scholar
  117. 117.
    Golic KG, Lindquist S (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509PubMedCrossRefGoogle Scholar
  118. 118.
    McLean PF, Cooley L (2013) Protein equilibration through somatic ring canals in Drosophila. Science 340:1445–1447PubMedCrossRefGoogle Scholar
  119. 119.
    Perrimon N (1984) Clonal analysis of dominant female-sterile germline-dependent mutations in Drosophila melanogaster. Genetics 108:927–939PubMedCentralPubMedGoogle Scholar
  120. 120.
    Perrimon N, Gans M (1983) Clonal analysis of the tissue specificity of recessive female-sterile mutations of Drosophila melanogaster using a dominant female-sterile mutation Fs(1)K1237. Dev Biol 100:365–373PubMedCrossRefGoogle Scholar
  121. 121.
    Chou TB, Perrimon N (1996) The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144:1673–1679PubMedCentralPubMedGoogle Scholar
  122. 122.
    Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170PubMedCrossRefGoogle Scholar
  123. 123.
    Karginov FV, Hannon GJ (2010) The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol Cell 37:7–19PubMedCentralPubMedCrossRefGoogle Scholar
  124. 124.
    Cong L, Ran FA, Cox D et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823PubMedCentralPubMedCrossRefGoogle Scholar
  125. 125.
    Ran FA, Hsu PD, Wright J et al (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308PubMedCentralPubMedCrossRefGoogle Scholar
  126. 126.
    Bassett AR, Liu JL (2014) CRISPR/Cas9 and genome editing in Drosophila. J Genet Genomics 41:7–19PubMedCrossRefGoogle Scholar
  127. 127.
    Gratz SJ, Cummings AM, Nguyen JN et al (2013) Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194:1029–1035PubMedCentralPubMedCrossRefGoogle Scholar
  128. 128.
    Gratz SJ, Ukken FP, Rubinstein CD et al (2014) Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196:961–971PubMedCentralPubMedCrossRefGoogle Scholar
  129. 129.
    Port F, Chen HM, Lee T et al (2014) Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc Natl Acad Sci U S A 111:2967–2976CrossRefGoogle Scholar
  130. 130.
    Hsu PD, Scott DA, Weinstein JA et al (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832PubMedCentralPubMedCrossRefGoogle Scholar
  131. 131.
    CRISPR Genome-Engineering. http://www.genome-engineering.org/crispr/

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Biological SciencesHunter College of the City University of New YorkNew YorkUSA
  2. 2.Molecular, Cellular, and Developmental Biology ProgramThe Graduate Center, CUNYNew YorkUSA

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