Chapter Two - Optogenetic approaches to investigate spatiotemporal signaling during development

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Abstract

Embryogenesis is coordinated by signaling pathways that pattern the developing organism. Many aspects of this process are not fully understood, including how signaling molecules spread through embryonic tissues, how signaling amplitude and dynamics are decoded, and how multiple signaling pathways cooperate to pattern the body plan. Optogenetic approaches can be used to address these questions by providing precise experimental control over a variety of biological processes. Here, we review how these strategies have provided new insights into developmental signaling and discuss how they could contribute to future investigations.

Section snippets

Optogenetic approaches

A major goal of developmental biology is to understand how specific tissues are reliably generated in different regions of the embryo. While decades of work have demonstrated that this process is orchestrated by signaling molecules and the pathways and genes they control, the specific underlying mechanisms remain incompletely characterized. A comprehensive understanding of embryogenesis requires deeper dissection of these mechanisms.

Optogenetic approaches use genetically encoded

Optogenetic applications in developmental signaling

Here, we highlight how the unique features of optogenetic systems have been beneficial for investigations of spatiotemporal signaling during development and suggest how these approaches could be further exploited. We use the foundational “French flag” model of tissue patterning as a framework to guide our discussion.

In the simplest contemporary conception of the French flag model, different concentration thresholds of a signaling molecule activate distinct sets of target genes and cell fates (

Practical considerations for optogenetic experiments

Thousands of light-responsive protein variants occur naturally, and many have been engineered to optimize specific features (Glantz et al., 2016; Losi et al., 2018). The choice of a light-responsive protein for a given application should be informed by several factors, including the reversibility, activation/inactivation wavelengths, and chromophore. The on/off kinetics of light-responsive proteins play a major role in an optogenetic system's behavior (Losi et al., 2018; Pudasaini, El-Arab, &

Conclusions and prospects

Advances in optogenetic methods over the last 10 years have introduced novel opportunities for developmental biology investigations. Optogenetic control over biological processes that are essential to embryogenesis, including signaling and gene expression, has been demonstrated in a range of in vitro and in vivo models, and insights into several patterning systems have already been gained using these approaches. In particular, the high degree of control offered by some optogenetic systems has

Acknowledgments

We are grateful to Harald Janovjak, Jared Toettcher, Daniel Čapek, Mohammad ElGamacy, Amit Landge, David Mörsdorf, Autumn Pomreinke, Hannes Preiß, Timothy Saunders, and Gary Soh, as well as the 2019 EMBO Practical Course on Optogenetics for helpful discussions. We thank Michal Rössler for the illustrations. This work was supported by the Max Planck Society and an HFSP Career Development Award (CDA00031/2013-C).

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