Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis

Abstract

Studies of the maternal processes that specify the Drosophila anteroposterior embryonic axis have yielded rich insight into various biological processes required for animal development. As the oocyte is a single cell with a single, largely quiescent nucleus, polarising and symmetry‐breaking events must be executed through molecular mechanisms other than transcriptional control. These include intercellular interactions such as signal transduction and differential cell adhesion. mRNA‐based mechanisms are also prominent in establishing the anteroposterior embryonic axis. Specific mRNAs become enriched at the anterior or posterior poles through motor‐protein driven microtubule‐dependent transport, or through bulk cytoplasmic movement followed by anchoring. Proteins encoded by these mRNAs establish gradients through spatiotemporal control of translation and by diffusion coupled with degradation.

  • Ovary structure determines the activities of polarising pathways that establish the anteroposterior embryonic axis.
  • Initial asymmetries correlate with unequal cell divisions, a polarised cytoskeleton and differential cell adhesion.
  • Germ cell – follicle cell interactions establish and maintain polarity in developing follicles.
  • Microtubule‐dependent mRNA localisation is critical to axis establishment.
  • Localised determinants initiate regulatory cascades that establish the anteroposterior body axis of the embryo and specify primordial germ cells.
  • Various ribonucleoprotein complexes (RNPs) are essential for germ line development and for axis formation.
  • Phase transition of proteins with intrinsically disordered domains are involved in the formation of several classes of these RNPs.

Keywords: anteroposterior axis determination; symmetry‐breaking events; oogenesis; polarity; directional cytoskeletal transport; RNA localisation; translational control

Figure 1. Oogenesis and key polarising events. Organisation of the ovary; for better visibility the germarium is shown enlarged. GSC‐derived cystoblasts undergo four rounds of mitosis, resulting in a 16 cell cyst. Cyst cells are connected by ring canals which persist throughout most of oogenesis. Initially, the fusome spans the cyst and is replaced by a polarised microtubule skeleton. Upon leaving the germarium, cysts are enveloped by follicle cells. Inductive Notch/Delta and Jak/Stat signalling originating from the adjacent, more mature, follicle leads to the DE‐cadherin‐dependent localisation of the oocyte to the posterior of the follicle. Grk‐dependent signalling and PAR protein activity establish polarity within the cyst. During mid‐oogenesis (stage 9/10), the microtubule network is anchored on the cortical actin cytoskeleton and points toward the ooplasm. This leads to initial localisation of bcd mRNA to the anterior and osk mRNA to the posterior of the oocyte. Upon commencement of nurse cell dumping and ooplasmic streaming, the bulk of RNPs is localised by diffusion and entrapment. Simplified cytoplasmic flow is indicated by arrows.
Figure 2. Organisation of a polar granule. Polar granules are huge RNP structures. Key proteins, including Osk, Vas, Tud and Aub, are distributed evenly through the structure. Key know mRNAs are organised in homotypic clusters which have a biased distribution: nos and pgc mRNAs tend to be more centrally located while pgc and gcl mRNAs are mostly found towards the periphery.
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References

Bastock R and St Johnston D (2008) Drosophila oogenesis. Current Biology 18: R1082–R1087.

Bilinski SM, Jaglarz MK and Tworzydlo W (2017) The pole (germ) plasm in insect oocytes. Results and Problems in Cellular Differentiation 63: 103–126.

Cai X, Fahmy K and Baumgartner S (2019) bicoid RNA localization requires the trans‐Golgi network. Hereditas 156: 30.

Clapp M and Marlow FL (2017) Acquisition of oocyte polarity. Results and Problems in Cellular Differentiation 63: 71–102.

De Keuckelaere E, Hulpiau P, Saeys Y, Berx G and van Roy F (2018) Nanos genes and their role in development and beyond. Cellular and Molecular Life Sciences 75: 1929–1946.

Dehghani M and Lasko P (2015) In vivo mapping of the functional regions of the DEAD‐box helicase Vasa. Biology Open 4: 450–462.

Dehghani M and Lasko P (2016) C‐terminal residues specific to Vasa among DEAD‐box helicases are required for its functions in piRNA biogenesis and embryonic patterning. Development, Genes, and Evolution 226: 401–412.

Dehghani M and Lasko P (2017) Multiple functions of the DEAD‐Box Helicase Vasa in Drosophila oogenesis. Results and Problems in Cellular Differentiation 63: 127–147.

Dold A, Han H, Liu N, et al. (2020) Makorin 1 controls embryonic patterning by alleviating Bruno1‐mediated repression of oskar translation. PLoS Genetics 16: e1008581.

Dufourt J, Bontonou G, Chartier A, et al. (2017) piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm. Nature Communications 8: 1305.

Eagle WVI, Yeboa‐Kordieh DK, Niepielko MG and Gavis ER (2018) Distinct cis‐acting elements mediate targeting and clustering of Drosophila polar granule mRNAs. Development 145: dev164657.

Gao M and Arkov AL (2013) Next generation organelles: structure and role of germ granules in the germline. Molecular Reproduction and Development 80: 610–623.

Gáspár I, Sysoev V, Komissarov A and Ephrussi A (2017) An RNA‐binding atypical tropomyosin recruits kinesin‐1 dynamically to oskar mRNPs. The EMBO Journal 36: 319–333.

Goldman CH and Gonsalvez GB (2017) The role of microtubule motors in mRNA localization and patterning within the Drosophila oocyte. Results and Problems in Cellular Differentiation 63: 149–168.

Guzikowski AR, Chen YS and Zid BM (2019) Stress‐induced mRNP granules: form and function of processing bodies and stress granules. Wiley Interdisciplinary Reviews: RNA 10 (3): e1524.

Hurd TR, Herrmann B, Sauerwald J, et al. (2016) Long Oskar controls mitochondrial inheritance in Drosophila melanogaster. Developmental Cell 39: 560–571.

Irion U and St Johnston D (2007) bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445: 554–558.

Jambór H, Surendranath V, Kalinka AT, et al. (2015) Systematic imaging reveals features and changing localization of mRNAs in Drosophila development. eLife 4: e05003.

Jeske M, Bordi M, Glatt S, et al. (2015) The crystal structure of the Drosophila germline inducer Oskar identifies two domains with distinct Vasa helicase and RNA‐binding activities. Cell Reports 12: 587–598.

Khuc Trong P, Doerflinger H, Dunkel J, St Johnston D and Goldstein RE (2015) Cortical microtubule nucleation can organise the cytoskeleton of Drosophila oocytes to define the anteroposterior axis. eLife 4: e06088.

Kilchert C, Sträßer K, Kunetsky V and Änkö ML (2020) From parts lists to functional significance‐RNA‐protein interactions in gene regulation. Wiley Interdisciplinary Reviews: RNA 11 (3): e1582.

Kistler KE, Trcek T, Hurd TR, et al. (2018) Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells. eLife 7: e37949.

Krishnakumar P, Riemer S, Perera R, et al. (2018) Functional equivalence of germ plasm organizers. PLoS Genetics 14: e1007696.

Kugler JM and Lasko P (2009) Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly 3: 15–28.

Kugler JM, Woo JS, Oh BH and Lasko P (2010) Regulation of Drosophila Vasa in vivo through paralogous cullin‐RING E3 ligase specificity receptors. Molecular and Cellular Biology 30: 1769–1782.

Lazzaretti D, Veith K, Kramer K, et al. (2016) The bicoid mRNA localization factor Exuperantia is an RNA‐binding pseudonuclease. Nature Structural and Molecular Biology 23: 705–713.

Lee J, Lee S, Chen C, Shim H and Kim‐Ha J (2016) shot regulates the microtubule reorganization required for localization of axis‐determining mRNAs during oogenesis. FEBS Letters 590: 431–444.

Lehmann R (2016) Germ plasm biogenesis – an Oskar‐centric perspective. Current Topics in Developmental Biology 116: 679–707.

Little SC, Sinsimer KS, Lee JJ, Wieschaus EF and Gavis ER (2015) Independent and coordinate trafficking of single Drosophila germ plasm mRNAs. Nature Cell Biology 17: 558–568.

Liu NK, Dansereau DA and Lasko P (2003) Fat facets interacts with Vasa in the Drosophila pole plasm and protects it from degradation. Current Biology 13: 1905–1909.

Lu W, Lakonishok M, Serpinskaya AS, et al. (2018) Ooplasmic flow cooperates with transport and anchorage in Drosophila oocyte posterior determination. Journal of Cell Biology 217: 3497–3511.

Lu W, Lakonishok M, Liu R, et al. (2020) Competition between kinesin‐1 and myosin‐V defines Drosophila posterior determination. eLife 9: e54216.

Nashchekin D, Fernandes AR and St Johnston D (2016) Patronin/Shot cortical foci assemble the noncentrosomal microtubule array that specifies the Drosophila anterior‐posterior axis. Developmental Cell 38: 61–72.

Niepielko MG, Eagle WVI and Gavis ER (2018) Stochastic seeding coupled with mRNA self‐recruitment generates heterogeneous Drosophila germ granules. Current Biology 28: 1872–1881.

Nott TJ, Petsalaki E, Farber P, et al. (2015) Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Molecular Cell 57: 936–947.

Quinlan ME (2016) Cytoplasmic streaming in the Drosophila oocyte. Annual Reviews of Cell and Developmental Biology 32: 173–195.

Ramat A, Garcia‐Silva MR, Jahan C, et al. (2020) The PIWI protein Aubergine recruits eIF3 to activate translation in the germ plasm. Cell Research. DOI: 10.1038/s41422‐020‐0294‐9.

Roth S and Lynch JA (2009) Symmetry breaking during Drosophila oogenesis. Cold Spring Harbor Perspectives in Biology 1 (2): a001891.

Rouget C, Papin C, Boureux A, et al. (2010) Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467: 1128–1132.

Sinsimer KS, Lee JJ, Thiberge SY and Gavis ER (2013) Germ plasm anchoring is a dynamic state that requires persistent trafficking. Cell Reports 5: 1169–1177.

Styhler S, Nakamura A and Lasko P (2002) Vasa localization requires the SPRY‐domain and SOCS box containing protein, Gustavus. Developmental Cell 3: 865–876.

Surkova S, Golubkova E, Mamon L and Samsonova M (2018) Dynamic maternal gradients and morphogenetic networks in Drosophila early embryo. Biosystems 173: 207–213.

Suyama R, Jenny A, Curado S, Pellis‐van Berkel W and Ephrussi A (2009) The actin‐binding protein Lasp promotes Oskar accumulation at the posterior pole of the Drosophila embryo. Development 136: 95–105.

Tanaka T, Kato Y, Matsuda K, Hanyu‐Nakamura K and Nakamura A (2011) Drosophila Mon2 couples Oskar‐induced endocytosis with actin remodeling for cortical anchorage of the germ plasm. Development 138: 2523–2532.

Trcek T, Grosch M, York A, et al. (2015) Drosophila germ granules are structured and contain homotypic mRNA clusters. Nature Communications 6: 7962.

Trcek T and Lehmann R (2019) Germ granules in Drosophila. Traffic 20: 650–660.

Trovisco V, Belaya K, Nashchekin D, et al. (2016) bicoid mRNA localises to the Drosophila oocyte anterior by random Dynein‐mediated transport and anchoring. eLife 5: e17537.

Vo HDL, Wahiduzzaman, Tindell SJ, et al. (2019) Protein components of ribonucleoprotein particles from Drosophila germ cells oligomerize and show distinct spatial organization during germline development. Scientific Reports 9: 19190.

Vourekas A, Alexiou P, Vrettos N, Maragkakis M and Mourelatos Z (2016) Sequence‐dependent but not sequence‐specific piRNA adhesion traps mRNAs to the germ plasm. Nature 531: 390–394.

Yang N, Yu Z, Hu M, et al. (2015) Structure of Drosophila Oskar reveals a novel RNA binding protein. Proceedings of the National Academy of Sciences of the United States of America 112: 11541–11546.

Further Reading

Bernard F, Lepesant JA and Guichet A (2018) Nucleus positioning within Drosophila egg chamber. Seminars in Cell & Developmental Biology 82: 25–33. Comprehensive review of nuclear positioning during oogenesis and its impact on axis specification and nurse cell dumping (see glossary).

Collart MA (2016) The Ccr‐4‐Not complex is a key regulator of eukaryotic gene expression. Wiley Interdisciplinary Reviews: RNA 7 (4): 438–454. Comprehensive review of the functions of the Ccr4‐Not complex (see glossary).

Czech B, Munafo M, Ciabrelli F, et al. (2018) piRNA‐guided genome defense: from biogenesis to silencing. Annual Review of Genetics 52: 131–157. Elaborate review on the piRNA pathways (see glossary) and how they function in genome protection.

Hershey JWB, Sonenberg N and Mathews MB (2019) Principles of translational control. Cold Spring Harbor Perspectives in Biology 11: a032607. General overview on translational control mechanisms.

Hinnant TD, Merkle JA and Ables ET (2020) Coordinating proliferation, polarity, and cell fate in the Drosophila female germline. Frontiers in Cell and Developmental Biology 8: 19. A comprehensive review on germ line cyst development including a detailed discussion of the fusome (see glossary).

Kloc M, Jedrzejowska I, Tworzydlo W and Bilinski SM (2014) Balbiani body, nuage and sponge bodies – the germ plasm pathway players. Arthropod Structure and Development 43: 341–348. Elaboration on different germ line specific structures, especially the Balbiani body (see glossary).

Lang CF and Munro E (2017) The PAR proteins: from molecular circuits to dynamic self‐stabilizing cell polarity. Development 144: 3405–3416. A comprehensive review on PAR proteins (see glossary), focussing on the pioneering model C. elegans but covering Drosophila as well.

Teixeira FK and Lehmann R (2019) Translational control during developmental transitions. Cold Spring Harbor Perspectives in Biology 11: a032987. Broad review on translational control in development.

Timmons AK, Mondragon AA, Schenkel CE, et al. (2016) Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary. Proceedings of the National Academy of Sciences of the United States of America 113: E1246–E1255. Elaborates on the programmed cell death program executed during nurse cell dumping (see glossary).

Yoshizawa T, Nozawa RS, Jia TZ, Saio T and Mori E (2020) Biological phase separation: cell biology meets biophysics. Biophysical Reviews. DOI: 10.1007/s12551‐020‐00680‐x. Comprehensive review on liquid‐liquid phase transitions.

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Kugler, Jan‐Michael, and Lasko, Paul(Aug 2020) Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029150]