An essential role for the RNA-binding protein Smaug during the<i>Drosophila</i>maternal-to-zygotic transition

Benoit, Béatrice; He, Congfen; Zhang, Fan; Votruba, Sarah M.; Tadros, Wael; Westwood, J. Timothy; Smibert, Craig; Lipshitz, Howard D.; Theurkauf, William E.

doi:10.1242/dev.031815

Cited by 133 publications

(215 citation statements)

References 52 publications

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“…Consistent with this hypothesis, increasing or decreasing the maternal dosage of the string and twine genes -and thus of maternal string and twine mRNA levels -results in an increase or decrease, respectively, in the number of nuclear cycles that occur prior to blastoderm cellularization (Edgar and Datar, 1996). Also consistent with this hypothesis, embryos produced by smaug mutant females, in which cell cycle mRNAs such as Cyclin A and B fail to be eliminated, continue to undergo very rapid nuclear cycles without slowing and pausing as in wild-type embryos (Benoit et al, 2009). …”

Section: Functions Of Maternal Transcript Destabilizationmentioning

confidence: 68%

“…miR-430 requires additional, zygotically produced, nonmiRNA factors to degrade a subset of its targets (Ferg et al, 2007). The D. melanogaster miR-309 family of miRNAs, which are synthesized zygotically in a SMG-dependent manner, participate in the destabilization of several hundred maternal mRNAs in a manner analogous to that of zebrafish miR-430 (Benoit et al, 2009;Bushati et al, 2008). Beyond these studies, it has been shown in D. melanogaster that genomic loci that map to different chromosome arms are required for the destabilization of distinct subsets of maternal mRNAs (De Renzis et al, 2007).…”

Section: Mechanisms Of Maternal Transcript Destabilizationmentioning

confidence: 99%

“…In D. melanogaster, transcription has been detected prior to the first wave of ZGA: genome wide, 30 genes are predicted to be transcribed during the first few nuclear cleavages, within the first 30 minutes after fertilization (Lecuyer et al, 2007). Microarray-based expression profiling studies -supplemented in D. melanogaster by genome-wide fluorescence in situ hybridization analyses (Lecuyer et al, 2007) -have begun to uncover the scope of ZGA: up to 15% of the genome in D. melanogaster (Benoit et al, 2009;De Renzis et al, 2007;Lecuyer et al, 2007), over 12% in zebrafish (Mathavan et al, 2005) and over 15% in mice (Hamatani et al, 2004). These values are likely to be underestimates (see Box 3).…”

Section: Dynamics and Scale Of Zygotic Genome Activationmentioning

confidence: 99%

“…SMG, which is translated upon egg activation and is required for the destabilization of the majority of maternal transcripts (Tadros et al, 2007), is essential for the vast majority of high-level transcription during ZGA (Benoit et al, 2009). The SMGdependent destruction of maternal mRNAs could time ZGA onset (Benoit et al, 2009) (Fig. 4).…”

Section: Maternal Clockmentioning

confidence: 99%

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The maternal-to-zygotic transition: a play in two acts

2009

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All animal embryos pass through a stage during which developmental control is handed from maternally provided gene products to those synthesized from the zygotic genome. This maternal-to-zygotic transition (MZT) has been extensively studied in model organisms, including echinoderms, nematodes, insects, fish,amphibians and mammals. In all cases, the MZT can be subdivided into two interrelated processes: first, a subset of maternal mRNAs and proteins is eliminated; second, zygotic transcription is initiated. The timing and scale of these two events differ across species, as do the cellular and morphogenetic processes that sculpt their embryos. In this article, we discuss conserved and distinct features within the two component processes of the MZT.

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Section: Functions Of Maternal Transcript Destabilizationmentioning

confidence: 68%

Section: Mechanisms Of Maternal Transcript Destabilizationmentioning

confidence: 99%

Section: Dynamics and Scale Of Zygotic Genome Activationmentioning

confidence: 99%

Section: Maternal Clockmentioning

confidence: 99%

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The maternal-to-zygotic transition: a play in two acts

2009

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“…S1 in the supplementary material), and prevents the production of larval cuticle. Smaug has recently been shown to be crucial for mediating the maternal-to-zygotic transition in Drosophila, and many of its additional targets are involved in regulating the cell cycle (Benoit et al, 2009). Our results with Nvsmaug indicate that many of the targets of Smaug regulation may have been conserved across holometabolan insect phylogeny.…”

Section: Research Article Nanos Function In Nasoniamentioning

confidence: 99%

Novel modes of localization and function of nanos in the wasp Nasonia

Lynch

Desplan

2010

Development

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SUMMARYAbdominal patterning in Drosophila requires the function of nanos (nos) to prevent translation of hunchback (hb) mRNA in the posterior of the embryo. nos function is restricted to the posterior by the translational repression of mRNA that is not incorporated into the posteriorly localized germ plasm during oogenesis. The wasp Nasonia vitripennis (Nv) undergoes a long germ mode of development very similar to Drosophila, although the molecular patterning mechanisms employed in these two organisms have diverged significantly, reflecting the independent evolution of this mode of development. Here, we report that although Nv nanos (Nv-nos) has a conserved function in embryonic patterning through translational repression of hb, the timing and mechanisms of this repression are significantly delayed in the wasp compared with the fly. This delay in Nv-nos function appears to be related to the dynamic behavior of the germ plasm in Nasonia, as well as to the maternal provision of Nv-Hb protein during oogenesis. Unlike in flies, there appears to be two functional populations of Nv-nos mRNA: one that is concentrated in the oosome and is taken up into the pole cells before evidence of Nv-hb repression is observed; another that forms a gradient at the posterior and plays a role in Nv-hb translational repression. Altogether, our results show that, although the embryonic patterning function of nos orthologs is broadly conserved, the mechanisms employed to achieve this function are distinct.

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Blastoderm Formation and Cellularisation inDrosophila melanogaster

Kotadia

Crest

Tram

et al. 2010

Encyclopedia of Life Sciences

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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.

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An essential role for the RNA-binding protein Smaug during theDrosophilamaternal-to-zygotic transition

Cited by 133 publications

References 52 publications

The maternal-to-zygotic transition: a play in two acts

The maternal-to-zygotic transition: a play in two acts

Novel modes of localization and function of nanos in the wasp Nasonia

Blastoderm Formation and Cellularisation inDrosophila melanogaster

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