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

Jan‐Michael Kugler, University of Copenhagen, Panum Institute, Copenhagen, Denmark
Paul Lasko, McGill University, Montréal, Québec, Canada

Published online: August 2020

DOI: 10.1002/9780470015902.a0029150

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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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).

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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.

Related Sub-Topics:

Intracellular and Extracellular Signalling | Genes, Molecules and Cellular Processes | Cell Cytoskeleton | Determination of Cell Fate | Gametogenesis and Fertilisation | Cellular Transport
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Article Title: Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis
 
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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]