Abstract
Many primary sensory cilia exhibit unique architectures that are critical for transduction of specific sensory stimuli. Although basic ciliogenic mechanisms are well described, how complex ciliary structures are generated remains unclear. Seminal work performed several decades ago provided an initial but incomplete description of diverse sensory cilia morphologies in C. elegans. To begin to explore the mechanisms that generate these remarkably complex structures, we have taken advantage of advances in electron microscopy and tomography, and reconstructed three-dimensional structures of fifty of sixty sensory cilia in the C. elegans adult hermaphrodite at high resolution. We characterize novel axonemal microtubule organization patterns, clarify structural features at the ciliary base, describe new aspects of cilia-glia interactions, and identify structures suggesting novel mechanisms of ciliary protein trafficking. This complete ultrastructural description of diverse cilia in C. elegans provides the foundation for investigations into underlying ciliogenic pathways, as well as contributions of defined ciliary structures to specific neuronal functions. DOI: http://dx.doi.org/10.7554/eLife.01948.001.
Highlights
Animals must sense and respond to multiple environmental cues over a wide range of signal intensities
The morphological and ultrastructural analyses presented here build on previous work (Ward et al, 1975; Ware et al, 1975; Perkins et al, 1986) to provide a complete 3D description of the anterior sensory anatomy of C. elegans at high resolution
These analyses reveal several novel features of C. elegans cilia in detail that will inform investigations into neuronal functions
Summary
Animals must sense and respond to multiple environmental cues over a wide range of signal intensities. The complexity of external cues is reflected in part in the remarkable diversity of sensory neuron morphologies and functions. Many major sensory neuron types contain microtubule (MT)-based primary cilia that house signal transduction molecules and are essential for the neurons’ sensory properties (Perkins et al, 1986; Inglis et al, 2007; McEwen et al, 2008; Ramamurthy and Cayouette, 2009; Pifferi et al, 2010). Vertebrate olfactory neurons contain a tuft of 6–17 cilia that emanate from the dendritic knobs and house olfactory signaling proteins (Menco, 1980; McEwen et al, 2008; Pifferi et al, 2010). Analysis of sensory cilia architecture, as well as their organization and interaction with supporting
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