Abstract
The assembly and maintenance of all cilia and flagella require intraflagellar transport (IFT) along the axoneme. IFT has been implicated in sensory and motile ciliary functions, but the mechanisms of this relationship remain unclear. Here, we used Chlamydomonas flagellar surface motility (FSM) as a model to test whether IFT provides force for gliding of cells across solid surfaces. We show that IFT trains are coupled to flagellar membrane glycoproteins (FMGs) in a Ca(2+)-dependent manner. IFT trains transiently pause through surface adhesion of their FMG cargos, and dynein-1b motors pull the cell towards the distal tip of the axoneme. Each train is transported by at least four motors, with only one type of motor active at a time. Our results demonstrate the mechanism of Chlamydomonas gliding motility and suggest that IFT plays a major role in adhesion-induced ciliary signaling pathways. DOI:http://dx.doi.org/10.7554/eLife.00744.001.
Highlights
Cilia and flagella are microtubule-based organelles that power the locomotion of many organisms, generate fluid flow over multiciliated surfaces, and mediate cell signaling (Liem et al, 2012)
We monitored the movement of individual image of the two channels (IFT) trains by using total internal reflection fluorescence (TIRF) illumination to image paralyzed-flagella mutant cells that had adhered to the glass surface with both flagella
Multicolor kymography analysis shows that the beads transiently dissociated from one IFT train, diffused for a period of time and bound to another IFT train (Figure 1A, Video 1) similar to the movement of extraflagellar particles observed along the flagellar membrane (Dentler, 2005)
Summary
Cilia and flagella are microtubule-based organelles that power the locomotion of many organisms, generate fluid flow over multiciliated surfaces, and mediate cell signaling (Liem et al, 2012). Several studies have suggested that IFT transports material between the cell body and the flagellar tip, and interacts dynamically with the flagellar membrane (Kozminski et al, 1993) to regulate diverse ciliary functions including motility, mating, sensing extracellular signals and influencing developmental decisions (Huangfu et al, 2003; Snell et al, 2004; Pedersen and Rosenbaum, 2008; Ishikawa and Marshall, 2011). It has remained unclear how transport of IFT trains underneath the flagellar membrane transmits force to components at the exterior of the flagellar membrane. Evidence supporting the role of IFT in gliding motility is indirect and the precise functions of IFT, molecular motors, FMG1-B and Ca2+ in FSM remain unclear
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