Abstract
With eight flagella of four different lengths, the parasitic protist Giardia is an ideal model to evaluate flagellar assembly and length regulation. To determine how four different flagellar lengths are maintained, we used live-cell quantitative imaging and mathematical modeling of conserved components of intraflagellar transport (IFT)-mediated assembly and kinesin-13-mediated disassembly in different flagellar pairs. Each axoneme has a long cytoplasmic region extending from the basal body, and transitions to a canonical membrane-bound flagellum at the 'flagellar pore'. We determined that each flagellar pore is the site of IFT accumulation and injection, defining a diffusion barrier functionally analogous to the transition zone. IFT-mediated assembly is length-independent, as train size, speed, and injection frequencies are similar for all flagella. We demonstrate that kinesin-13 localization to the flagellar tips is inversely correlated to flagellar length. Therefore, we propose a model where a length-dependent disassembly mechanism controls multiple flagellar lengths within the same cell.
Highlights
Eukaryotic flagella and cilia are dynamic, compartmentalized microtubule (MT) organelles that facilitate motility and chemosensation, and direct hydrodynamic flow during development (Brooks and Wallingford, 2014; Pazour and Witman, 2003)
The cytoplasmic axonemal regions span from the basal body to flagellar pore (Figure 1A, shaded; Figure 1B) and membrane-bound axonemal regions span from the flagellar pore to flagellar tip (Figure 1A, colored)
Giardia trophozoites are a unique and ideal model to test the mechanisms of flagellar length control that enable multiciliated cells to possess flagella with different lengths
Summary
Eukaryotic flagella and cilia (used interchangeably) are dynamic, compartmentalized microtubule (MT) organelles that facilitate motility and chemosensation, and direct hydrodynamic flow during development (Brooks and Wallingford, 2014; Pazour and Witman, 2003). As well as IFT components and flagellar assembly mechanisms, likely predate the radiation of all extant lineages (Ishikawa, 2017; Sung and Leroux, 2013) due to widespread conservation in diverse unicellular flagellates ranging from Chlamydomonas, Tetrahymena, and Trypanosoma to the ciliated cell types of invertebrates and mammals (Buisson et al, 2013; Hao and Scholey, 2009; Kozminski et al, 1993) Despite these conserved elements, there is considerable variation in flagellar number, structure and function in microbial and multicellular eukaryotes (Avidor-Reiss et al, 2017; Ishikawa, 2017).
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