Abstract
The primary cilium is nucleated by the mother centriole-derived basal body (BB) via as yet poorly characterized mechanisms. BBs have been reported to degenerate following ciliogenesis in the C. elegans embryo, although neither BB architecture nor early ciliogenesis steps have been described in this organism. In a previous study (Doroquez et al., 2014), we described the three-dimensional morphologies of sensory neuron cilia in adult C. elegans hermaphrodites at high resolution. Here, we use serial section electron microscopy and tomography of staged C. elegans embryos to demonstrate that BBs remodel to support ciliogenesis in a subset of sensory neurons. We show that centriolar singlet microtubules are converted into BB doublets which subsequently grow asynchronously to template the ciliary axoneme, visualize degeneration of the centriole core, and define the developmental stage at which the transition zone is established. Our work provides a framework for future investigations into the mechanisms underlying BB remodeling.
Highlights
Cilia are evolutionarily conserved microtubule (MT)-based organelles that play key roles in regulating embryonic development, sensory signaling, and motility among other cellular functions (Goetz and Anderson, 2010; Green and Mykytyn, 2010; Yildiz and Khanna, 2012; Falk et al, 2015)
We described the three-dimensional morphologies of sensory cilia in the nose of C. elegans hermaphrodites at high resolution using serial section transmission electron microscopy and serial section electron tomography of high pressure-frozen and freezesubstituted (HPF-FS) adult animals (Doroquez et al, 2014)
We find that singlet MTs (sMTs) of centrioles in early embryos contain hook-like appendages that remodel to dMTs during basal body (BB) maturation and prior to axoneme elongation, and template the dMTs of the ciliary axoneme
Summary
Cilia are evolutionarily conserved microtubule (MT)-based organelles that play key roles in regulating embryonic development, sensory signaling, and motility among other cellular functions (Goetz and Anderson, 2010; Green and Mykytyn, 2010; Yildiz and Khanna, 2012; Falk et al, 2015). Centrioles/BBs are cylindrical structures that can be comprised of a radially symmetric array of MT singlets, doublets, or triplets depending on the species and cellular context (Azimzadeh and Marshall, 2010; Winey and O’Toole, 2014; Carvalho-Santos et al, 2011; Gottardo et al, 2015; Gonzalez et al, 1998; Jana et al, 2016) It remains unclear whether centrioles of distinct ultrastructural organization transition to BBs and nucleate cilia via similar or distinct mechanisms
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