Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans

Abstract

Background information The current consensus on cilia development posits that the ciliary transition zone (TZ) is formed via extension of nine centrosomal microtubules. In this model, TZ structure remains unchanged in microtubule number throughout the cilium life cycle. This model does not however explain structural variations of TZ structure seen in nature, and could also lend itself to the misinterpretation that deviations from nine-doublet microtubule ultrastructure represent an abnormal phenotype. Thus, a better understanding of events that occur at the TZ in vivo during metazoan development is required. Results To address this issue, we characterized ultrastructure of two types of sensory cilia in developing Caenorhabditis elegans. We discovered that, in cephalic male (CEM) and inner labial quadrant (IL2Q) sensory neurons, ciliary TZs are structurally plastic and remodel from one structure to another during animal development. The number of microtubules doublets forming the TZ can be increased or decreased over time, depending on cilia type. Both cases result in structural TZ intermediates different from TZ in cilia of adult animals. In CEM cilia, axonemal extension and maturation occurs concurrently with TZ structural maturation. Conclusions and Significance Our work extends the current model to include the structural plasticity of metazoan transition zone, which can be structurally delayed, maintained or remodeled in cell type-specific manner.

The connectome of the Caenorhabditis elegans pharynx

“…Three types of ultrastructural specializations are present, classified as apical (Figure 4c), unexposed (Figure 4d), and embedded (Figure 4e). Pharyngeal sensory endings are primitive in appearance and do not include basal bodies, Y-links, axonemes, or cilia (Akella et al, 2019;Li et al, 2004;Perkins, Hedgecock, Thomson, & Culotti, 1986). vesicles and short cytoskeletal fibrils, but no organized axoneme (Perkins et al, 1986).…”

Sensory cilia act as a specialized venue for regulated extracellular vesicle biogenesis and signaling

“…In the wild type (J) and the pkd-2 mutant (K) CIL- The CEM neurons express genes required for ciliary axoneme specialization and sensory function at the L4 stage upon sexual maturation. 11,[17][18][19][20] To avoid protein accumulation as a secondary consequence of aging, we examined PKD-2 and CIL-7 localization at the L4 stage to directly detect ciliary localization or EV shedding defects. In wild-type L4 cilia, PKD-2 and CIL-7 reached the ciliary tip and were shed as EVs into the environment (Figure 3A).…”

TMEM218 dysfunction causes ciliopathies, including Joubert and Meckel syndromes

“…The dense TZ protein network is organized into concentric ring structures and can be functionally separated into modules, although we are just beginning to appreciate the plasticity of this region. 8 , 29 – 31 At the core of the TZ, JS-associated proteins RPGRIP1L, CEP290, and CC2D2A facilitate localization of other TZ components. NPHP1 and NPHP4 localize more peripherally.…”