DisAp-dependent striated fiber elongation is required to organize ciliary arrays

Galati, Domenico F.; Bonney, Stephanie; Kronenberg, Zev; Clarissa, Christina; Yandell, Mark; Elde, Nels C.; Jerka‐Dziadosz, Maria; Giddings, Thomas H.; Frankel, Joseph; Pearson, Chad G.

doi:10.1083/jcb.201409123

Cited by 42 publications

(124 citation statements)

References 59 publications

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“…In the former case, hydrodynamic coupling between flagella is sufficient (12), but, in the latter (especially for obligate autotrophs), there is far greater incentive for efficient swimming to be robust despite hydrodynamic perturbations. Even in arrays of mammalian cilia, ciliary roots and basal feet structures continue to provide additional resistance to fluid stresses (22,81).…”

Section: Discussionmentioning

confidence: 99%

“…Such strategies are vital not only in microswimmers bearing few flagella but also in ciliary arrays. In mice, defects in structures known as basal feet can cause ciliopathies (21), whereas the striated (kinetodesmal) fibers in Tetrahymena help maintain BB orientation and resist hydrodynamic stresses (22). Insights from primitive flagellates may thus have significant broader implications.…”

Section: Significancementioning

confidence: 99%

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Coordinated beating of algal flagella is mediated by basal coupling

Wan

Goldstein

2016

Proc. Natl. Acad. Sci. U.S.A.

166

193

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Cilia and flagella often exhibit synchronized behavior; this includes phase locking, as seen in Chlamydomonas, and metachronal wave formation in the respiratory cilia of higher organisms. Since the observations by Gray and Rothschild of phase synchrony of nearby swimming spermatozoa, it has been a working hypothesis that synchrony arises from hydrodynamic interactions between beating filaments. Recent work on the dynamics of physically separated pairs of flagella isolated from the multicellular alga Volvox has shown that hydrodynamic coupling alone is sufficient to produce synchrony. However, the situation is more complex in unicellular organisms bearing few flagella. We show that flagella of Chlamydomonas mutants deficient in filamentary connections between basal bodies display markedly different synchronization from the wild type. We perform micromanipulation on configurations of flagella and conclude that a mechanism, internal to the cell, must provide an additional flagellar coupling. In naturally occurring species with 4, 8, or even 16 flagella, we find diverse symmetries of basal body positioning and of the flagellar apparatus that are coincident with specific gaits of flagellar actuation, suggesting that it is a competition between intracellular coupling and hydrodynamic interactions that ultimately determines the precise form of flagellar coordination in unicellular algae.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Coordinated beating of algal flagella is mediated by basal coupling

Wan

Goldstein

2016

Proc. Natl. Acad. Sci. U.S.A.

166

193

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“…This has been successful in various model organisms, including the ciliates Tetrahymena and Paramecium (Sarin et al 2008;Blumenstiel et al 2009; Birkeland et al 2010;Cuperus et al 2010;Galati et al 2014;Marker et al 2014;A. Turkewitz and J. Gaertig, personal communication).…”

Section: Identifying Mutations By Ngsmentioning

confidence: 99%

“…It was previously difficult to identify the mutations associated with a phenotype due to difficulties in producing genomewide libraries to rescue mutant phenotypes. However, next generation sequencing (NGS) is now an effective tool to rapidly identify mutations in Tetrahymena and in other genomes (Galati et al 2014;Schneeberger 2014). The development of NGS to identify mutations created in Tetrahymena forward genetic screens greatly increases the power of this system for new mechanistic research.…”

Section: Forward and Reverse Geneticsmentioning

confidence: 99%

“…To map by sequencing, the mutant is backcrossed to the wild-type parent and a panel of homozygous F 2 meiotic segregants is obtained by UPC. Alternatively, F 1 progeny of different mating types can be crossed to one another and F 2 's displaying the mutant phenotype can be selected (Galati et al 2014;A. Turkewitz, personal communication).…”

Section: Identifying Mutations By Ngsmentioning

confidence: 99%

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Tetrahymenaas a Unicellular Model Eukaryote: Genetic and Genomic Tools

2016

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Tetrahymena thermophila is a ciliate model organism whose study has led to important discoveries and insights into both conserved and divergent biological processes. In this review, we describe the tools for the use of Tetrahymena as a model eukaryote, including an overview of its life cycle, orientation to its evolutionary roots, and methodological approaches to forward and reverse genetics. Recent genomic tools have expanded Tetrahymena's utility as a genetic model system. With the unique advantages that Tetrahymena provide, we argue that it will continue to be a model organism of choice.

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Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

et al. 2015

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SUMMARY There are six members of the tubulin superfamily in eukaryotes [1]. Alpha- and beta-tubulin form a heterodimer that polymerizes to form microtubules, and gamma-tubulin nucleates microtubules as a component of the gamma-tubulin ring complex. Alpha-, beta-, and gamma-tubulin are conserved in all eukaryotes. In contrast, delta- and epsilon-tubulin are conserved in many, but not all, eukaryotes and are associated with centrioles, although their molecular function is unclear [2–7]. Zeta-tubulin is the sixth and final member of the tubulin superfamily, and is largely uncharacterized. We find that zeta-, epsilon-, and delta-tubulin form an evolutionarily co-conserved module, the ZED module, that has been lost at several junctions in eukaryotic evolution, and that zeta- and delta-tubulin are evolutionarily interchangeable. Humans lack zeta-tubulin, but have delta-tubulin. In Xenopus multiciliated cells, zeta-tubulin is a component of the basal foot, a centriolar appendage that connects centrioles to the apical cytoskeleton, and co-localizes there with epsilon-tubulin. Depletion of zeta-tubulin results in disorganization of centriole distribution and polarity in multiciliated cells. In contrast with multiciliated cells, zeta-tubulin in cycling cells does not localize to centrioles and is associated with the TRiC/CCT cytoplasmic chaperone complex. We conclude that zeta-tubulin facilitates interactions between the centrioles and the apical cytoskeleton as a component of the basal foot in differentiated cells, and propose that the ZED tubulins are important for centriole functionalization and orientation of centrioles with respect to cellular polarity axes.

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DisAp-dependent striated fiber elongation is required to organize ciliary arrays

Abstract: DisAp is a novel kinetodesmal fiber component that is essential for force-dependent fiber elongation and the alignment of basal body orientation in multiciliary arrays.

Cited by 42 publications

References 59 publications

Coordinated beating of algal flagella is mediated by basal coupling

Coordinated beating of algal flagella is mediated by basal coupling

Tetrahymenaas a Unicellular Model Eukaryote: Genetic and Genomic Tools

Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

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