Abstract
The guidance of axons to their correct targets is a critical step in development. The C. elegans pharynx presents an attractive system to study neuronal pathfinding in the context of a developing organ. The worm pharynx contains relatively few cells and cell types, but each cell has a known lineage and stereotyped developmental patterns. We found that extension of the M1 pharyngeal axon, which spans the entire length of the pharynx, occurs in two distinct phases. The first proximal phase does not require genes that function in axon extension (unc-34, unc-51, unc-115, and unc-119), whereas the second distal phase does use these genes and is guided in part by the adjacent g1P gland cell projection. unc-34, unc-51, and unc-115 had incompletely penetrant defects and appeared to act in conjunction with the g1P cell for distal outgrowth. Only unc-119 showed fully penetrant defects for the distal phase. Mutations affecting classical neuronal guidance cues (Netrin, Semaphorin, Slit/Robo, Ephrin) or adhesion molecules (cadherin, IgCAM) had, at best, weak effects on the M1 axon. None of the mutations we tested affected the proximal phase of M1 elongation. In a forward genetic screen, we isolated nine mutations in five genes, three of which are novel, showing defects in M1, including axon overextension, truncation, or ectopic branching. One of these mutations appeared to affect the generation or differentiation of the M1 neuron. We conclude that M1 axon extension is a robust process that is not completely dependent on any single guidance mechanism.
Highlights
The guidance of axons to their correct targets is a critical step in development
To test whether the M1 axon phenotype that we observed in unc-51, unc-34, and unc-115 mutants was a secondary result of defects of the g1P gland projection, we examined gland shape in these mutants
In this work, we explored the development of the C. elegans M1 motor neuron, which extends almost the entire length of the pharynx, as a model of how axons are extended within a simple structure, the pharynx
Summary
The guidance of axons to their correct targets is a critical step in development. The C. elegans pharynx presents an attractive system to study neuronal pathfinding in the context of a developing organ. The NSM and M2 pharyngeal neurons use unusual growth cone–independent mechanisms (Axang et al 2008; Morck et al 2003; Pilon 2008), extending for part of their journeys using the “fishing line” paradigm (Bray 1984; Chada et al 1997; Heidemann et al 1995; Zheng et al 1991) In this model, the neuron soma (“the fish”) may pull out the axon (“the line”) as the cell body moves away from an initial attachment point. Amphid dendrites extend by a similar mechanism (Heiman and Shaham 2009)
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