Abstract
In living organisms, self-organised waves of signalling activity propagate spatiotemporal information within tissues. During the development of the largest component of the visual processing centre of the Drosophila brain, a travelling wave of proneural gene expression initiates neurogenesis in the larval optic lobe primordium and drives the sequential transition of neuroepithelial cells into neuroblasts. Here, we propose that this 'proneural wave' is driven by an excitable reaction-diffusion system involving epidermal growth factor receptor (EGFR) signalling interacting with the proneural gene l'sc. Within this framework, a propagating transition zone emerges from molecular feedback and diffusion. Ectopic activation of EGFR signalling in clones within the neuroepithelium demonstrates that a transition wave can be excited anywhere in the tissue by inducing signalling activity, consistent with a key prediction of the model. Our model illuminates the physical and molecular underpinnings of proneural wave progression and suggests a generic mechanism for regulating the sequential differentiation of tissues.
Highlights
The development of multicellular organisms relies on a multitude of transient coordination processes that provide the spatiotemporal cues for cell fate decision-making and thereby ensure that tissues are specified with the correct size, pattern and composition (Perrimon et al, 2012; Oates et al, 2012; Sato et al, 2013)
It was proposed that sequential induction of epidermal growth factor receptor (EGFR) signalling is responsible for the progression of the proneural wave (Yasugi et al, 2008)
We noted that the dynamics of EGFR signalling alone has features that are sufficient to enable such a sequential induction and produce a travelling front of EGFR signalling activity; a feature notably absent in recent attempts to model the proneural wave, which require further components to stabilise the propagating EGFR signalling front (Sato et al, 2016)
Summary
The development of multicellular organisms relies on a multitude of transient coordination processes that provide the spatiotemporal cues for cell fate decision-making and thereby ensure that tissues are specified with the correct size, pattern and composition (Perrimon et al, 2012; Oates et al, 2012; Sato et al, 2013). Large-scale patterning is engineered by self-organised concentration waves of biomolecular fate determinants that travel across tissues through intercellular exchange and the regulation of gene expression Such travelling waves, which are viable carriers of spatiotemporal information, are a ubiquitous feature of developmental pattern formation, where they arise through different underlying mechanisms, from coordinated intracellular oscillations (Oates et al, 2012; Jorg et al, 2015; Hubaud et al, 2017; Verd et al, 2018) to self-organised reaction-diffusion processes (Lubensky et al, 2011; Formosa-Jordan et al, 2012; Fried et al, 2016; Gavish et al, 2016; Corson et al, 2017).
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