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A Precise Bicoid Gradient Is Nonessential during Cycles 11–13 for Precise Patterning in the Drosophila Blastoderm

Lucchetta, Elena M. and Vincent, Meghan E. and Ismagilov, Rustem F. (2008) A Precise Bicoid Gradient Is Nonessential during Cycles 11–13 for Precise Patterning in the Drosophila Blastoderm. PLoS ONE, 3 (11). e3651. ISSN 1932-6203. PMCID PMC2578877. https://resolver.caltech.edu/CaltechAUTHORS:20130821-160725343

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[img] Video (AVI) (Movie S1. Movies show the dynamics of cytoplasmic movement in developing embryos. To facilitate visualization of the movement at the surface of the embryo, black particle tracers were added to the images by using the image analysis software) - Supplemental Material
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[img] Video (AVI) (Movie S2. A movie shows the dynamics of nuclear movement in a developing embryo in a microfluidic device at uniform temperature of 23°C. The nuclei were visualized by using the expression of histone-eGFP (blue)) - Supplemental Material
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[img] Video (AVI) (Movie S3. A movie shows the dynamics of nuclear movement in a developing embryo in a microfluidic device exposed to a temperature step with anterior (left) at 20°C and posterior (right) at 27°C. The nuclei were visualized by the expression of histone-eGFP) - Supplemental Material
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[img] Video (AVI) (Movie S4. A movie shows a partial nuclear division cycle only in the anterior (left, cool) half of an embryo developing in a microfluidic device exposed to a temperature step with the anterior (left) at 20°C and posterior (right) at 27°C) - Supplemental Material
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[img] Video (AVI) (Movie S5. A movie shows the dynamics of the Bcd gradient in a developing embryo in a microfluidic device at uniform temperature of 23°C. Embryos were expressing Bcd-eGFP (green)) - Supplemental Material
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[img] Video (AVI) (Movie S6. A movie shows the dynamics of the Bcd gradient in a developing embryo in a microfluidic device exposed to a temperature step with anterior (left) at 20°C and posterior (right) at 27°C. Embryos were expressing Bcd-eGFP (green)) - Supplemental Material
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Abstract

Background: During development, embryos decode maternal morphogen inputs into highly precise zygotic gene expression. The discovery of the morphogen Bicoid and its profound effect on developmental programming in the Drosophila embryo has been a cornerstone in understanding the decoding of maternal inputs. Bicoid has been described as a classical morphogen that forms a concentration gradient along the antero-posterior axis of the embryo by diffusion and initiates expression of target genes in a concentration-dependent manner in the syncytial blastoderm. Recent work has emphasized the stability of the Bicoid gradient as a function of egg length and the role of nuclear dynamics in maintaining the Bicoid gradient. Bicoid and nuclear dynamics were observed but not modulated under the ideal conditions used previously. Therefore, it has not been tested explicitly whether a temporally stable Bicoid gradient prior to cellularization is required for precise patterning. Principal Findings: Here, we modulate both nuclear dynamics and the Bicoid gradient using laminar flows of different temperature in a microfluidic device to determine if stability of the Bicoid gradient prior to cellularization is essential for precise patterning. Dramatic motion of both cytoplasm and nuclei was observed prior to cellularization, and the Bicoid gradient was disrupted by nuclear motion and was highly abnormal as a function of egg length. Despite an abnormal Bicoid gradient during cycles 11–13, Even-skipped patterning in these embryos remained precise. Conclusions: These results indicate that the stability of the Bicoid gradient as a function of egg length is nonessential during syncytial blastoderm stages. Further, presumably no gradient formed by simple diffusion on the scale of egg length could be responsible for the robust antero-posterior patterning observed, as severe cytoplasmic and nuclear motion would disrupt such a gradient. Additional mechanisms for how the embryo could sense its dimensions and interpret the Bicoid gradient are discussed.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0003651DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2578877/PubMed CentralArticle
ORCID:
AuthorORCID
Ismagilov, Rustem F.0000-0002-3680-4399
Additional Information:Copyright: © 2008 Lucchetta et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. We thank Eric F. Wieschaus for providing the Bcd-eGFP stock, Gerold Schubiger for providing the His2AvD-GFP stock, Nipam H. Patel and Manfred Frasch for providing antibodies, Nipam H. Patel and Kevin P. White for helpful discussions, and Elizabeth W. Boyd for contributions to writing and editing this manuscript. We thank referees for helpful suggestions. Author Contributions: Conceived and designed the experiments: EML RFI. Performed the experiments: EML MEV. Analyzed the data: EML. Contributed reagents/materials/analysis tools: RFI. Wrote the paper: EML RFI. Funding: This work was funded by NIH Grant No. R01 GM077331 and the Yen Postdoctoral Fellowship (E.M.L.). Competing interests: The authors have declared that no competing interests exist.
Funders:
Funding AgencyGrant Number
NIHR01 GM077331
Yen Postdoctoral FellowshipUNSPECIFIED
Issue or Number:11
PubMed Central ID:PMC2578877
Record Number:CaltechAUTHORS:20130821-160725343
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130821-160725343
Official Citation:Lucchetta EM, Vincent ME, Ismagilov RF (2008) A Precise Bicoid Gradient Is Nonessential during Cycles 11–13 for Precise Patterning in the Drosophila Blastoderm. PLoS ONE 3(11): e3651. doi:10.1371/journal.pone.0003651
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:40833
Collection:CaltechAUTHORS
Deposited By: Whitney Barlow
Deposited On:27 Aug 2013 20:42
Last Modified:06 Jul 2020 22:40

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