Blastoderm Formation and Cellularisation in Drosophila melanogaster

Abstract

Immediately following fertilisation in Drosophila and many other arthropods, the embryo undergoes a series of rapid syncytial nuclear divisions. These divisions are driven by maternally supplied components and occur in the absence of zygotic transcription. Unlike typical cell divisions, these divisions alternate between S and M phases, resulting in cell cycles that last only from 10 to 25 min. After four rounds of division, the nuclei undergo axial expansion, a process that relies on microfilaments. Subsequently migration of the nuclei to the cortex relies on microtubules. Once at the cortex, the nuclear divisions occur on a single plane and rely on partial cleavage furrows to maintain an even distribution. The cortical nuclear divisions continue until the mid‐blastula transition (MBT), at which time cellularisation results in the formation of a multicellular embryo.

Key Concepts:

  • Fertilisation triggers a series of events that induces the first mitotic cycle, a gonomeric division between the male and female pronucleus.

  • After fertilisation, the embryo undergoes 13 synchronous divisions within a syncytium.

  • Divisions 10–13 occur at the cortex of the embryo and require reorganisation of actin and membrane into metaphase furrows.

  • At cycle 14, the cell cycle pauses and cellularisation occurs forming individual somatic cells.

  • Cellularisation, a key feature of the mid‐blastula transition, marks the time at which zygotic transcription occurs and maternal products are degraded.

Keywords: Drosophila; embryo; syncytial; blastoderm; cellularisation; mid‐blastula transition; fertilisation; furrow

Figure 1.

Fertilisation and pronuclear fusion. Sperm fertilises the meiosis I arrested egg. The egg then undergoes two meiotic divisions to generate three polar bodies and one pronucleus (blue). During this process, the male nucleus sheds its protamines (red) and deposits histones (purple) to become replication competent. Following this, chromosomes condense, the nuclear envelope breaks down and fusion with the female pronucleus occurs. (This figure was modelled after Figure in Landmann et al. .)

Figure 2.

Early nuclear divisions and migration during Drosophila embryogenesis. Cycle 1 is initiated after fusion of the male and female pronuclei. During divisions 1–3, nuclei divide in a sphere at the anterior of the embryo. During divisions 4–6, nuclei divide and spread out along the anterior–posterior axis (axial expansion). Nuclei migrate to the cortex of the embryo during divisions 8–10 (cortical migration). Pole cells form at the posterior end of the embryo (cycle 9), whereas yolk nuclei remain in the interior. After four rounds of cortical syncytial divisions, during interphase of nuclear cycle 14, invagination of the plasma membrane around each nucleus produces a cellularised embryo.

Figure 3.

Metaphase furrow formation. (a) During interphase, the actin (green) concentrates into apical caps centred above each cortical nucleus (blue) and its apically positioned centrosomes (yellow). (b) As the nuclei progress into prophase, the centrosomes migrate towards opposite poles and the actin caps undergo a dramatic redistribution to outline each nucleus and its associated separated centrosome pair. (c) At metaphase, the furrows invaginate to a depth of approximately 10 μm to surround each spindle both apically and laterally, but not basally. Vesicles (black circles) transport actin puncta (green) that fuse with the growing furrow. (d) and (e) During late anaphase and telophase, the metaphase furrows rapidly regress.

Figure 4.

Live imaging of metaphase furrow formation. Surface confocal sections highlight the reorganisation of interphase actin caps above each nucleus into metaphase furrows. Actin caps are distinct from one another during interphase, where gaps (*) can be observed. By metaphase, actin caps have expanded laterally to fill these gaps and invagination into metaphase furrows has reached maximum length (∼10 μm). Metaphase furrows retract by telophase, reforming apical caps. Actin (green) and microtubules (red). Scale bar=10 μm.

Figure 5.

Formation of the cellularisation furrows. (a) Cellularisation begins with actin (green) concentrated at the cortex above each nucleus and apical centrosome pair (yellow). Astral microtubules extend basally and form a cage within which nuclear elongation occurs. (b) The plasma membrane initiates invagination and actin is concentrated at the cortex and the leading edge of the furrow. (c) The slow phase of furrow invagination is initiated. Golgi‐ and recycling endosome‐derived vesicles drive furrow elongation. (d) Furrows invaginate rapidly once they have passed the fully elongated nuclei. (e) Once furrows have reached a depth of 35 μm, the leading edge relies on actin–myosin‐based contraction (red) to pinch off basally. Adherens junctions (brown) connect neighbouring cellular membranes.

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Further Reading

Foe VE, Odell GM and Edgar BA (1993) Mitosis and morphogenesis in the Drosophila embryo. In: Bate M and Arias AM (eds) The Development of Drosophila melanogaster. Plainview, NY: Cold Spring Harbor Laboratory Press.

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Tadros W and Lipshitz HD (2005) Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Developmental Dynamics 3: 593–608.

Tadros W and Lipshitz HD (2009) The maternal‐to‐zygotic transition: a play in two acts. Development 18: 3033–3042.

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Kotadia, Shaila, Crest, Justin, Tram, Uyen, Riggs, Blake, and Sullivan, William(Sep 2010) Blastoderm Formation and Cellularisation in Drosophila melanogaster. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001071.pub2]