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Blastoderm Formation and Introductory article Cellularisation in Article Contents . Drosophila’s Unusual Syncytial Blastoderm Drosophila melanogaster . Fertilisation and Preblastoderm Cycles . Blastoderm Cycles Shaila Kotadia, University of California at Santa Cruz, Santa Cruz, California, USA Online posting date: 15th September 2010 Justin Crest, University of California at Santa Cruz, Santa Cruz, California, USA Uyen Tram, The Ohio State University, Columbus, Ohio, USA Blake Riggs, San Francisco State University, San Francisco, California, USA William Sullivan, University of California at Santa Cruz, Santa Cruz, California, USA Immediately following fertilisation in Drosophila and of some 6000 nuclei in a common cytoplasm (Foe and many other arthropods, the embryo undergoes a series of Alberts, 1983; Zalokar and Erk, 1976). At interphase of rapid syncytial nuclear divisions. These divisions are dri- nuclear cycle 14, these nuclei are packaged into individual ven by maternally supplied components and occur in the cells in a process known as cellularisation. This rapid devel- opment is achieved by several attributes of the early embryo. absence of zygotic transcription. Unlike typical cell div- First, the embryo is endowed with an abundance of mater- isions, these divisions alternate between S and M phases, nally supplied products, which allows it to bypass zygotic resulting in cell cycles that last only from 10 to 25 min. transcription during the first several divisions. Second, the After four rounds of division, the nuclei undergo axial nuclear division cycles alternate between M and S phases. expansion, a process that relies on microfilaments. Sub- Lastly, nuclear division is uncoupled from cytokinesis. Thus, sequently migration of the nuclei to the cortex relies on the initial division cycles proceed rapidly, ranging from 10 to microtubules. Once at the cortex, the nuclear divisions 25 min, compared to the typical cell cycle duration of 24 h. occur on a single plane and rely on partial cleavage fur- Once fertilisation and fusion of the male and female pronuclei rows to maintain an even distribution. The cortical occur, the syncytial cycles are initiated. During these div- nuclear divisions continue until the mid-blastula transi- isions, the nuclei undergo a precisely orchestrated pattern of tion (MBT), at which time cellularisation results in the migration and movements. During the first three divisions, the nuclei remain clustered in a ball at the anterior third of the formation of a multicellular embryo. embryo. During nuclear cycles 4–6, in a process called axial expansion, the nuclei become evenly distributed along the length of the embryo. Nuclear migration to the cortex begins during nuclear cycle 8 and the first nuclei arrive at the pos- terior end of the cortex at nuclear cycle 9. These nuclei are the Drosophila’s Unusual Syncytial germline precursors and protrude through the plasma membrane to form pole cells during nuclear cycle 10. Most of Blastoderm the remaining nuclei arrive synchronously at the cortex dur- ing interphase of nuclear cycle 10. These cortical nuclei Overview undergo four more divisions and finally cellularise during interphase of nuclear cycle 14. Space is limited during the Like in many other insects, early embryonic development in syncytial divisions. This problem is particularly acute during Drosophila melanogaster is rapid and occurs in a syncytium. the cortical divisions when thousands of nuclei are rapidly The first 13 nuclear divisions are completed in just over 3 h dividing in a confined monolayer. In spite of the crowding, and occur in the absence of cytokinesis, producing an embryo embryogenesis is an extremely precise process. This article highlights classic and recent studies that illuminate the mechanisms driving these events. ELS subject area: Developmental Biology How to cite: Fertilisation and Preblastoderm Cycles Kotadia, Shaila; Crest, Justin; Tram, Uyen; Riggs, Blake; and Sullivan, William (September 2010) Blastoderm Formation and Cellularisation in Drosophila melanogaster. In: Encyclopedia of Life Sciences (ELS). John Fertilisation and the first mitotic cycle Wiley & Sons, Ltd: Chichester. After mating, a Drosophila female typically stores 300–500 DOI: 10.1002/9780470015902.a0001071.pub2 sperms in specialised sperm storage organs called the ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net 1 Blastoderm Formation and Cellularisation in Drosophila melanogaster spermathecae and seminal receptacle. This supply of sperm by nuclear envelope reformation, S phase and fusion with enables the female to fertilise mature oocytes in the uterus the female pronucleus (Callaini and Riparbelli, 1996; for up to 2 weeks without remating. Sperms are released Longo, 1985). from the storage organs and enter the egg through a special As in many other species, germline centrosome inherit- opening at the anterior end called the micropyle. Although ance in Drosophila is asymmetric. During oogenesis, cen- egg activation and fertilisation occur simultaneously, the trioles are lost but the surrounding pericentriolar material former does not depend on sperm entry but rather on (PCM) is retained (Riparbelli and Callaini, 1996). Con- hydration of the egg during passage through the oviduct versely during spermiogenesis, the sperm retains core cen- (Horner and Wolfner, 2008). Egg activation induces a triolar components in its basal body but lacks PCM number of events including release from the metaphase (Wilson et al., 1997). Upon fertilisation, the basal body meiosis I arrest (Figure 1). Completion of meiosis produces relies on maternally supplied components for transforma- four haploid meiotic products arranged perpendicularly tion into a centriole and reformation of the PCM. with respect to the plasma membrane. The innermost Although the sperm is normally required for centriole nucleus migrates towards the interior while the remaining formation, recent work demonstrates that all the com- three nuclei cluster to form polar bodies enveloped by ponents necessary for centriole formation are present in the microtubules. Immediately following fertilisation, the egg, as overexpression of core centriolar proteins induces nuclear envelope of the sperm nucleus is removed and the centriole formation in the absence of fertilisation (Peel chromatin undergoes extensive remodelling replacing et al., 2007; Rodrigues-Martins et al., 2007). protamines with maternally supplied histones (Jayar- The first mitotic division in Drosophila is known as a amaiah Raja and Renkawitz-Pohl, 2005). This is followed gonomeric division because the maternal and paternal Paternal Meiosis I nuclear metaphase envelope arrest removed Protamines removed Core histones deposited Nuclear envelope formation Replication Cdk1 activation Polar bodies Nuclear envelope breakdown, chromosome Cycle 1 mitosis condensation Mitosis 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 5 in Landmann et al. (2009).) 2 ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net Blastoderm Formation and Cellularisation in Drosophila melanogaster genomes remain separated on the metaphase plate expansion, the nuclei become evenly distributed along the (Callaini and Riparbelli, 1996). Once the male and female length of the embryo. This process is sensitive to cytocha- pronuclei reside next to each other, the newly assembled lasin but not colcemid, indicating that the underlying sister centrosomes separate to form the poles of the spindle. mechanism requires microfilaments, but is independent of This is immediately followed by nuclear envelope break- microtubules (von Dassow and Schubiger, 1994). Muta- down and entry into metaphase. Large sections of the tional analysis demonstrates that cell cycle-regulated nuclear envelope remain intact, however, maintaining the rounds of actin–myosin based cortical contraction are separation of maternal and paternal chromosome com- required for driving axial expansion. It is thought that the plements through anaphase. Subsequently, in telophase, cortical contractions drive cytoplasmic streaming, which in the male and female nuclei join to form two diploid zygotic turn drives axial expansion. See also: Actin and Actin nuclei that proceed to the syncytial embryonic divisions. Filaments During these early cycles, the centrosome plays a key role Mitotic cycling in generating astral microtubules that orient and prevent collisions between neighbouring syncytial nuclei (Rothwell In Drosophila, as well as in many other insects, the first and Sullivan, 2000). Embryos containing defective cen- embryonic divisions after fertilisation are syncytial. That trosomes that fail to produce the robust astral microtubule is, nuclear divisions occur in the absence of cytokinesis. arrays develop functional mitotic spindles and undergo Drosophila has 13 syncytial mitotic cycles, the first 9 of several rounds of division but eventually large numbers of which occur in the centre of the embryo and are referred to fused nuclei are often observed. as the preblastoderm cycles. These cycles consist of only
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