Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm.

Raphaël Aguillon,Pascale Dufourcq,Julie Batut,Thomas F Schilling,Patrick Blader,Arul Subramanian,Romain Madelaine

doi:10.7554/elife.32041

Raphaël Aguillon, Pascale Dufourcq + Show 5 more

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https://doi.org/10.7554/elife.32041

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Abstract

The zebrafish olfactory epithelium comprises a variety of neuronal populations, which are thought to have distinct embryonic origins. For instance, while ciliated sensory neurons arise from preplacodal ectoderm (PPE), previous lineage tracing studies suggest that both Gonadotropin releasing hormone 3 (Gnrh3) and microvillous sensory neurons derive from cranial neural crest (CNC). We find that the expression of Islet1/2 is restricted to Gnrh3 neurons associated with the olfactory epithelium. Unexpectedly, however, we find no change in Islet1/2+ cell numbers in sox10 mutant embryos, calling into question their CNC origin. Lineage reconstruction based on backtracking in time-lapse confocal datasets, and confirmed by photoconversion experiments, reveals that Gnrh3 neurons derive from the anterior PPE. Similarly, all of the microvillous sensory neurons we have traced arise from preplacodal progenitors. Our results suggest that rather than originating from separate ectodermal populations, cell-type heterogeneity is generated from overlapping pools of progenitors within the preplacodal ectoderm.

Highlights

A fundamental question in developmental neurobiology is how different neuronal subtypes arise from fields of pluripotent progenitors
The number and position of these Islet1/2+ cells resembles expression of gonadotropin releasing hormone 3 (Gopinath et al, 2004). To determine if they are the same cells, we examined expression of Islet1/2 in a transgenic line expressing enhanced GFP under the control of the gnrh3 promoter, which recapitulates the endogenous expression of gnrh3 associated with the olfactory epithelium (Abraham et al, 2008)
Our results reveal a complete overlap between enhanced GFP (eGFP) expression from the Tg(gnrh3:eGFP) transgene and Islet1/2 (Figure 1A)

Summary

Introduction

A fundamental question in developmental neurobiology is how different neuronal subtypes arise from fields of pluripotent progenitors. At the end of gastrulation, the anterior neural plate border of the zebrafish embryo gives rise to two specialized regions of ectoderm: the preplacodal ectoderm (PPE) that will produce the cranial placodes, and the cranial neural crest (CNC). CNC cells delaminate and migrate throughout the head, where they have been reported to contribute to a large number of cell types, including sensory and neurosecretory cells associated with the olfactory system (Whitlock et al, 2003; Saxena et al, 2013). This dual embryonic (PPE/ CNC) origin for olfactory neurons in zebrafish may have critical developmental and functional consequences

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