Decoding temporal interpretation of the morphogen Bicoid in the early Drosophila embryo

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Abstract

Morphogen gradients provide essential spatial information during development. Not only the local concentration but also duration of morphogen exposure is critical for correct cell fate decisions. Yet, how and when cells temporally integrate signals from a morphogen remains unclear. Here, we use optogenetic manipulation to switch off Bicoid-dependent transcription in the early Drosophila embryo with high temporal resolution, allowing time-specific and reversible manipulation of morphogen signalling. We find that Bicoid transcriptional activity is dispensable for embryonic viability in the first hour after fertilization, but persistently required throughout the rest of the blastoderm stage. Short interruptions of Bicoid activity alter the most anterior cell fate decisions, while prolonged inactivation expands patterning defects from anterior to posterior. Such anterior susceptibility correlates with high reliance of anterior gap gene expression on Bicoid. Therefore, cell fates exposed to higher Bicoid concentration require input for longer duration, demonstrating a previously unknown aspect of Bicoid decoding.

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Anqi Huang

Mechanobiology Institute, National University of Singapore, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
Christopher Amourda

Mechanobiology Institute, National University of Singapore, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5173-0159
Shaobo Zhang

Mechanobiology Institute, National University of Singapore, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
Nicholas S Tolwinski

Division of Science, Yale-NUS College, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
Timothy E Saunders

Mechanobiology Institute, National University of Singapore, Singapore, Singapore

For correspondence
dbsste@nus.edu.sg

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5755-0060

Funding

National Research Foundation Singapore

Timothy E Saunders

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations of the Agri-Food and Veterinary Authority of Singapore (Ref. NEA/CLU/16-0008).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.