Regulation of the pattern of basal bodies within the oral apparatus of Tetrahymena thermophila

Development ◽  
1982 ◽  
Vol 69 (1) ◽  
pp. 83-105
Author(s):  
Julita Bakowska ◽  
Joseph Frankel ◽  
E. Marlo Nelsen
Keyword(s):  
Tetrahymena Thermophila ◽  
Complete Loss ◽  
Basal Bodies ◽  
Spatial Features ◽  
Temporal Discontinuity ◽  
Real Change ◽  
Spatial Terms ◽  
Sequential Processes ◽  
Oral Development ◽  
Size Relation

The number and arrangement of basal bodies included in the four compound ciliary organelles making up the mature oral apparatus of Tetrahymena thermophila ordinarily vary only slightly. Severe starvation brings about formation of oral structures with a reduced number of basal bodies within these organelles, and sometimes with a complete loss of one of the component organelles. Such reductions are stringently specified in spatial terms, but they do not represent simple and proportional shrinkage of the organelle complex. Instead, certain spatial features remain essentially unaltered, while others undergo major quantitative reductions, resulting in large changes in the internal proportions of the structures. This selective regulation can be explained in terms of the different parallel and sequential processes taking place during the development of this organelle complex. There is also no strict proportionality between the size of the oral apparatus and that of the cell; instead, oral apparatuses become relatively larger as cells become smaller. This is due in part to the inherent temporal discontinuity of oral development, but there is probably also a real change in the oral/body size relation at the time of oral development. The ‘French flag’ rule fails when applied to the relative sizes and internal proportions of organelle systems in this and in other ciliates.

Mutational analysis of patterning of oral structures in Tetrahymena

Development ◽  
1984 ◽  
Vol 82 (1) ◽  
pp. 67-95
Author(s):  
Joseph Frankel ◽  
E. Marlo Nelsen ◽  
Julita Bakowska ◽  
Leslie M. Jenkins
Keyword(s):  
Mutational Analysis ◽  
Tetrahymena Thermophila ◽  
The State ◽  
The Other ◽  
Basal Bodies ◽  
Ciliated Protozoan ◽  
Vertebrate Limb ◽  
Spatial Configurations ◽  
Oral Development ◽  
Mutant Cells

The ciliary arrays of the oral apparatus of the ciliated protozoan Tetrahymena thermophila each have their own unique ‘pattern signature’, which varies little so long as the number of arrays remains the same. In this study, we analyse the consequence of increases in the number of these arrays (membranelles) brought about by certain mutations. In oral apparatuses of mutant cells, the addition of a membranelle is associated with specific alterations in at least one of the other membranelles. The features that are altered include the relative lengths of membranelles, the state of ciliation of basal bodies located at specific positions within these membranelles, and the spatial configurations resulting from displacement of ciliary units during late oral development. The final organization of each membranelle depends upon its relativeposition along the length of the oral apparatus. This indicates that the membranelles are not individually ‘named’ by the organism, and suggests that the unit of pattern organizationis the membranelle field as a whole. In the Discussion, we consider means for testing whether thesame underlying idea might also apply to multicellular systems, such as the vertebrate limb, in which spatially ordered differences appear to be superimposed upon a fundamental repeating pattern.

scholarly journals The Two SAS-6 Homologs in Tetrahymena thermophila Have Distinct Functions in Basal Body Assembly

2009 ◽  
Vol 20 (6) ◽  
pp. 1865-1877 ◽  
Author(s):  
Brady P. Culver ◽  
Janet B. Meehl ◽  
Thomas H. Giddings ◽  
Mark Winey
Keyword(s):  
Basal Body ◽  
Structural Component ◽  
Tetrahymena Thermophila ◽  
Basal Bodies ◽  
Hub And Spoke ◽  
Structural Role ◽  
Higher Eukaryotes ◽  
Centriole Assembly ◽  
Cilia And Flagella

Cilia and flagella are structurally and functionally conserved organelles present in basal as well as higher eukaryotes. The assembly of cilia requires a microtubule based scaffold called a basal body. The ninefold symmetry characteristic of basal bodies and the structurally similar centriole is organized around a hub and spoke structure termed the cartwheel. To date, SAS-6 is one of the two clearly conserved components of the cartwheel. In some organisms, overexpression of SAS-6 causes the formation of supernumerary centrioles. We questioned whether the centriole assembly initiation capacity of SAS-6 is separate from or directly related to its structural role at the cartwheel. To address this question we used Tetrahymena thermophila, which expresses two SAS-6 homologues, TtSAS6a and TtSAS6b. Cells lacking either TtSAS6a or TtSAS6b are defective in new basal body assembly. TtSas6a localizes to all basal bodies equally, whereas TtSas6b is enriched at unciliated and assembling basal bodies. Interestingly, overexpression of TtSAS6b but not TtSAS6a, led to the assembly of clusters of new basal bodies in abnormal locations. Our data suggest a model where TtSAS6a and TtSAS6b have diverged such that TtSAS6a acts as a structural component of basal bodies, whereas TtSAS6b influences the location of new basal body assembly.

scholarly journals Sfr1, a Tetrahymena thermophila Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

mSphere ◽  
2016 ◽  
Vol 1 (6) ◽  
Author(s):  
Westley Heydeck ◽  
Alexander J. Stemm-Wolf ◽  
Janin Knop ◽  
Christina C. Poh ◽  
Mark Winey
Keyword(s):  
Basal Body ◽  
Binding Proteins ◽  
Tetrahymena Thermophila ◽  
Binding Protein ◽  
Extensive Study ◽  
Basal Bodies ◽  
Content Type ◽  
Inhibitory Role ◽  
Body Production

ABSTRACT Basal bodies and centrioles are structurally similar and, when rendered dysfunctional as a result of improper assembly or maintenance, are associated with human diseases. Centrins are conserved and abundant components of both structures whose basal body and centriolar functions remain incompletely understood. Despite the extensive study of centrins in Tetrahymena thermophila, little is known about how centrin-binding proteins contribute to centrin’s roles in basal body assembly, stability, and orientation. The sole previous study of the large centrin-binding protein family in Tetrahymena revealed a role for Sfr13 in the stabilization and separation of basal bodies. In this study, we found that Sfr1 localizes to all Tetrahymena basal bodies and complete genetic deletion of SFR1 leads to overproduction of basal bodies. The uncovered inhibitory role of Sfr1 in basal body production suggests that centrin-binding proteins, as well as centrins, may influence basal body number both positively and negatively. Basal bodies are essential microtubule-based structures that template, anchor, and orient cilia at the cell surface. Cilia act primarily in the generation of directional fluid flow and sensory reception, both of which are utilized for a broad spectrum of cellular processes. Although basal bodies contribute to vital cell functions, the molecular contributors of their assembly and maintenance are poorly understood. Previous studies of the ciliate Tetrahymena thermophila revealed important roles for two centrin family members in basal body assembly, separation of new basal bodies, and stability. Here, we characterize the basal body function of a centrin-binding protein, Sfr1, in Tetrahymena. Sfr1 is part of a large family of 13 proteins in Tetrahymena that contain Sfi1 repeats (SFRs), a motif originally identified in Saccharomyces cerevisiae Sfi1 that binds centrin. Sfr1 is the only SFR protein in Tetrahymena that localizes to all cortical row and oral apparatus basal bodies. In addition, Sfr1 resides predominantly at the microtubule scaffold from the proximal cartwheel to the distal transition zone. Complete genomic knockout of SFR1 (sfr1Δ) causes a significant increase in both cortical row basal body density and the number of cortical rows, contributing to an overall overproduction of basal bodies. Reintroduction of Sfr1 into sfr1Δ mutant cells leads to a marked reduction of cortical row basal body density and the total number of cortical row basal bodies. Therefore, Sfr1 directly modulates cortical row basal body production. This study reveals an inhibitory role for Sfr1, and potentially centrins, in Tetrahymena basal body production. IMPORTANCE Basal bodies and centrioles are structurally similar and, when rendered dysfunctional as a result of improper assembly or maintenance, are associated with human diseases. Centrins are conserved and abundant components of both structures whose basal body and centriolar functions remain incompletely understood. Despite the extensive study of centrins in Tetrahymena thermophila, little is known about how centrin-binding proteins contribute to centrin’s roles in basal body assembly, stability, and orientation. The sole previous study of the large centrin-binding protein family in Tetrahymena revealed a role for Sfr13 in the stabilization and separation of basal bodies. In this study, we found that Sfr1 localizes to all Tetrahymena basal bodies and complete genetic deletion of SFR1 leads to overproduction of basal bodies. The uncovered inhibitory role of Sfr1 in basal body production suggests that centrin-binding proteins, as well as centrins, may influence basal body number both positively and negatively.

scholarly journals Microtubule glycylation promotes basal body attachment to the cell cortex

2019 ◽  
Author(s):  
Anthony D. Junker ◽  
Adam W. J. Soh ◽  
Eileen T. O’Toole ◽  
Janet B. Meehl ◽  
Mayukh Guha ◽  
...  
Keyword(s):  
Light Microscopy ◽  
Tetrahymena Thermophila ◽  
Hydrodynamic Flow ◽  
Cell Cortex ◽  
Basal Bodies ◽  
Post Translational Modifications ◽  
Summary Statement ◽  
Motile Cilia ◽  
Em Tomography ◽  
Cortical Cytoskeleton

ABSTRACTMotile cilia generate directed hydrodynamic flow that is important for the motility of cells and extracellular fluids. To optimize directed hydrodynamic flow, motile cilia are organized and oriented into a polarized array. Basal bodies (BB) nucleate and position motile cilia at the cell cortex. Cytoplasmic BB-associated microtubules are conserved structures that extend from BBs. Using the ciliate, Tetrahymena thermophila, combined with EM-tomography and light microscopy, we show that BB-appendage microtubules assemble coincident with new BB assembly and are attached to the cell cortex. These BB-appendage microtubules are specifically marked with post translational modifications of tubulin, including glycylation. Mutations that prevent glycylation shorten BB-appendage microtubules and disrupt BB positioning and cortical attachment. Consistent with the attachment of BB-appendage microtubules to the cell cortex for BB positioning, mutations that disrupt the cellular cortical cytoskeleton similarly disrupt the cortical attachment and positioning of BBs. In summary, BB-appendage microtubules promote the organization of ciliary arrays through attachment to the cell cortex.SUMMARY STATEMENTBasal bodies position motile cilia at the cell cortex. This study finds tubulin glycylation to promote BB-associated microtubule elongation and structural attachment of basal bodies to the cell’s cortical cytoskeleton.

scholarly journals  -tubulin is essential in Tetrahymena thermophila for the assembly and stability of basal bodies

2013 ◽  
Vol 126 (15) ◽  
pp. 3441-3451 ◽  
Author(s):  
I. Ross ◽  
C. Clarissa ◽  
T. H. Giddings ◽  
M. Winey
Keyword(s):  
Tetrahymena Thermophila ◽  
Basal Bodies

scholarly journals The LisH Domain-Containing N-Terminal Fragment is Important for the Localization, Dimerization, and Stability of Katnal2 in Tetrahymena

Cells ◽  
2020 ◽  
Vol 9 (2) ◽  
pp. 292
Author(s):  
Ewa Joachimiak ◽  
Ewa Waclawek ◽  
Michal Niziolek ◽  
Anna Osinka ◽  
Hanna Fabczak ◽  
...  
Keyword(s):  
Functional Analysis ◽  
Amino Acid ◽  
Amino Acid Sequence ◽  
Catalytic Domain ◽  
Tetrahymena Thermophila ◽  
Basal Bodies ◽  
Amino Acid Sequence Homology ◽  
Terminal Fragment ◽  
Wide Range ◽  
Microtubular Structures

Katanin-like 2 protein (Katnal2) orthologs have a tripartite domain organization. Two highly conserved regions, an N-terminal LisH (Lis-homology) domain and a C-terminal AAA catalytic domain, are separated by a less conserved linker. The AAA domain of Katnal2 shares the highest amino acid sequence homology with the AAA domain of the canonical katanin p60. Katnal2 orthologs are present in a wide range of eukaryotes, from protists to humans. In the ciliate Tetrahymena thermophila, a Katnal2 ortholog, Kat2, co-localizes with the microtubular structures, including basal bodies and ciliary outer doublets, and this co-localization is sensitive to levels of microtubule glutamylation. The functional analysis of Kat2 domains suggests that an N-terminal fragment containing a LisH domain plays a role in the subcellular localization, dimerization, and stability of Kat2.

scholarly journals Basal Body Duplication and Maintenance Require One Member of the Tetrahymena thermophila Centrin Gene Family

2005 ◽  
Vol 16 (8) ◽  
pp. 3606-3619 ◽  
Author(s):  
Alexander J. Stemm-Wolf ◽  
Garry Morgan ◽  
Thomas H. Giddings ◽  
Erin A. White ◽  
Robb Marchione ◽  
...  
Keyword(s):  
Basal Body ◽  
Calcium Binding ◽  
Tetrahymena Thermophila ◽  
Essential Gene ◽  
Expression Patterns ◽  
Spindle Pole ◽  
The Other ◽  
Basal Bodies ◽  
Spindle Pole Bodies ◽  
Ef Hand

Centrins, small calcium binding EF-hand proteins, function in the duplication of a variety of microtubule organizing centers. These include centrioles in humans, basal bodies in green algae, and spindle pole bodies in yeast. The ciliate Tetrahymena thermophila contains at least four centrin genes as determined by sequence homology, and these have distinct localization and expression patterns. CEN1's role at the basal body was examined more closely. The Cen1 protein localizes primarily to two locations: one is the site at the base of the basal body where duplication is initiated. The other is the transition zone between the basal body and axoneme. CEN1 is an essential gene, the deletion of which results in the loss of basal bodies, which is likely due to defects in both basal body duplication and basal body maintenance. Analysis of the three other centrins indicates that two of them function at microtubule-rich structures unique to ciliates, whereas the fourth is not expressed under conditions examined in this study, although when artificially expressed it localizes to basal bodies. This study provides evidence that in addition to its previously known function in the duplication of basal bodies, centrin is also important for the integrity of these organelles.

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