Abstract
Little is known about proneural gene function during olfactory neurogenesis in zebrafish. Here, we show that the zebrafish Atonal genes neurogenin1 (neurog1) and neurod4 are redundantly required for development of both early-born olfactory neurons (EONs) and later-born olfactory sensory neurons (OSNs). We show that neurod4 expression is initially absent in neurog1 mutant embryos but recovers and is sufficient for the delayed development of OSN. By contrast, EON numbers are significantly reduced in neurog1 mutant embryos despite the recovery of neurod4 expression. Our results suggest that a shortened time window for EON development causes this reduction; the last S-phase of EON is delayed in neurog1 mutant embryos but mutant EONs are all post-mitotic at the same stage as EONs in wild-type embryos. Finally, we show that expression of certain genes, such as robo2, is never detected in neurog1 mutant EONs. Failure of robo2 expression to recover correlates with defects in the fasciculation of neurog1 mutant olfactory axonal projections and in the organisation of proto-glomeruli because projections arrive at the olfactory bulb that are reminiscent of those in robo2 mutant embryos. We conclude that the duration of proneural expression in EON progenitors is crucial for correct development of the zebrafish olfactory system.
Highlights
The nervous system is established via a tightly controlled series of events, known as neurogenesis, which assures that the appropriate subtypes of neurons are born in the correct places and numbers, and at the correct times during embryogenesis
Tg(8.4neurog1:gfp) is a marker of early-born olfactory neurons in the zebrafish olfactory placode The expression of the proneural gene neurogenin1 at the border between the neural and non-neural ectoderm in the anterior part of the neural plate suggests that this basic helix-loop-helix transcription factor is involved in the development of earlyborn olfactory neurons and/or olfactory sensory neurons (Blader et al, 1997)
This transgene only recapitulates a part of the overall neurog1 expression pattern, the expression of neurog1 transcripts overlaps with the GFP driven by the transgene in the olfactory system at early stages
Summary
The nervous system is established via a tightly controlled series of events, known as neurogenesis, which assures that the appropriate subtypes of neurons are born in the correct places and numbers, and at the correct times during embryogenesis. The conservation of genes homologous to Drosophila proneural genes, such as members of the neurogenin (neurog) and acheatescute like (ascl) families, indicates that similar mechanisms are at work in vertebrates (Bertrand et al, 2002). The olfactory system has proven to be an attractive model for studying the role of proneural genes during vertebrate neurogenesis. Olfactory sensory neurons (OSN) are born in the sensory epithelium, which is itself derived from a pair of epidermal thickenings, or placodes, located on either side of the anterior neural plate (Cuschieri and Bannister, 1975a; Cuschieri and Bannister, 1975b; Smart, 1971). Loss-of-function studies in mice have shown that the sequential activity of members of the Ascl and Neurog families of proneural genes are required for the majority of OSN that develop.
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