The SM19 gene, required for duplication of basal bodies in Paramecium, encodes a novel tubulin, η-tubulin

Ruiz, Françoise; Krzywicka, Anna; Klotz, Catherine; Keller, Anne‐Marie; Cohen, Jean; Balavoine, Guillaume; Beisson, Janine

doi:10.1016/s0960-9822(00)00804-6

Cited by 66 publications

(66 citation statements)

References 22 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Entire gene modules are retained initially as duplicates with redundant functions, but some of them will evolve to derived ones if there is no need other than stoichiometry for maintaining the redundancy. One example of neo-functionalization is provided by d-and g-tubulins, paralogues of the old WGD, which have distinct functions in the assembly (d-tubulin 33 ) or duplication (g-tubulin 34 ) of ciliary basal bodies. g-Tubulin is known only in ciliates, whereas d-tubulin is conserved in eukaryotes that perpetuate the centriolar structure.…”

Section: Wgds In Genome Evolutionmentioning

confidence: 99%

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Aury

Jaillon

Duret

et al. 2006

Nature

Self Cite

759

836

View full text Add to dashboard Cite

The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.Ciliates are unique among unicellular organisms in that they separate germline and somatic functions 1 . Each cell harbours two kinds of nucleus, namely silent diploid micronuclei and highly polyploid macronuclei. The latter are unusual in that they contain an extensively rearranged genome streamlined for expression and divide by a non-mitotic process. Only micronuclei undergo meiosis to perpetuate genetic information; the macronuclei are lost at each sexual generation and develop anew from the micronuclear lineage.In Paramecium the exact number of micronuclear chromosomes (more than 50) and the structures of their centromeres and telomeres remain unknown. During macronuclear development, these chromosomes are amplified to about 800 copies and undergo two types of DNA elimination event. Tens of thousand of short, unique copy elements (internal eliminated sequences) are removed by a precise mechanism that leads to the reconstitution of functional genes 2 .Transposable elements and other repeated sequences are removed by an imprecise mechanism leading either to chromosome fragmentation and de novo telomere addition or to variable internal deletions 3 . These rearrangements occur after a few rounds of endoreplication, leading to some heterogeneity in the sequences abutting the imprecisely eliminated regions 3 . The sizes of the resulting, acentric macronuclear chromosomes range from 50-1,000 kilobases (kb) as measured by pulsed-field gel electrophoresis. Because the sexual process of autogamy results in an entirely homozygous genotype 4 , the macronuclear DNA that was sequenced was genetically homogeneous.The Paramecium genome sequence The Paramecium macronuclear genome sequence was established with the use of a whole-genome shotgun and assembly strategy. Paired-end sequencing of plasmid and bacterial artificial chromosome (BAC) clones provided a coverage of 13 genome equivalents (Supplementary Table S1). We assembled the sequence reads with Arachne 5 in 1,907 contigs connected in 697 scaffolds of size greater than 2 kb, giving a total coverage of 72...

show abstract

Section: Wgds In Genome Evolutionmentioning

confidence: 99%

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Aury

Jaillon

Duret

et al. 2006

Nature

Self Cite

759

836

View full text Add to dashboard Cite

show abstract

“…In Chlamydomonas and Paramecium [Garreau de Loubresse et al, 2001] mutation or knockdown of the gene for d tubulin results in defects in C tubule polymerization. In Paramecium, h tubulin is necessary for basal body duplication [Ruiz et al, 2000]. A mutation in the gene encoding this tubulin leads to cells with progressive loss of basal bodies.…”

Section: Unique Centriolar Proteinsmentioning

confidence: 99%

Evolution and persistence of the cilium

Satir

Guerra

Bell

2007

Cell Motil. Cytoskeleton

View full text Add to dashboard Cite

The origin of cilia, a fundamental eukaryotic organelle, not present in prokaryotes, poses many problems, including the origins of motility and sensory function, the origins of nine-fold symmetry, of basal bodies, and of transport and selective mechanisms involved in ciliogenesis. We propose the basis of ciliary origin to be a self-assembly RNA enveloped virus that contains unique tubulin and tektin precursors. The virus becomes the centriole and basal body, which would account for the self-assembly and self-replicative properties of these organelles, in contrast to previous proposals of spirochaete origin or endogenous differentiation, which do not readily account for the centriole or its properties. The viral envelope evolves into a sensory bud. The host cell supplies the transport machinery and molecular motors to construct the axoneme. Polymerization of cytoplasmic microtubules in the 9 1 0 axoneme completes the 9 1 2 pattern. Cell Motil. Cytoskeleton 64: 906-913, 2007. ' 2007

show abstract

“…Gamma tubulin is also ubiquitous and likely emerged early, to function as a nucleating site that helps determine microtubule polarity and distribution. Additional tubulin isoforms delta and epsilon are ubiquitous among organisms with triplet microtubules, and the formation of triplet microtubules, essential for the function of basal bodies, has been shown to require both delta and epsilon tubulin in Chlamydomonas 25,26 and both epsilon 27 and the less ubiquitous eta tubulin 28 in Paramecium. The presence of these tubulin isoforms in members of both the unikont and bikont clades 17,29 argues for their evolution prior to the divergence of eukaryotes.…”

Section: Evolution Of Tubulin Dynein and Kinesinmentioning

confidence: 99%

The Evolution of Eukaryotic Cilia and Flagella as Motile and Sensory Organelles

Mitchell

Advances in Experimental Medicine and Biology

185

152

View full text Add to dashboard Cite

Eukaryotic cilia and flagella are motile organelles built on a scaffold of doublet microtubules and powered by dynein ATPase motors. Some thirty years ago, two competing views were presented to explain how the complex machinery of these motile organelles had evolved. Overwhelming evidence now refutes the hypothesis that they are the modified remnants of symbiotic spirochaetelike prokaryotes, and supports the hypothesis that they arose from a simpler cytoplasmic microtubule-based intracellular transport system. However, because intermediate stages in flagellar evolution have not been found in living eukaryotes, a clear understanding of their early evolution has been elusive. Recent progress in understanding phylogenetic relationships among present day eukaryotes and in sequence analysis of flagellar proteins have begun to provide a clearer picture of the origins of doublet and triplet microtubules, flagellar dynein motors, and the 9+2 microtubule architecture common to these organelles. We summarize evidence that the last common ancestor of all eukaryotic organisms possessed a 9+2 flagellum that was used for gliding motility along surfaces, beating motility to generate fluid flow, and localized distribution of sensory receptors, and trace possible earlier stages in the evolution of these characteristics. Keywordscilia; flagella; motility; axoneme; microtubule; dynein; intraflagellar transport; central pair; radial spoke; tubulin Evidence for the presence of a 9+2, motile, sensory organelle in the last common eukaryotic ancestor As summarized in Figure 1, typical cilia and flagella (hereafter called flagella, there being no consistent structural or functional difference between organelles with these two designations) are motile projections oriented perpendicular to the cell surface, but they vary in length, in number per cell, and in the patterns of motility that they produce. They are composed of a cylinder (the axoneme) of nine doublet microtubules surrounding two single microtubules and are covered by the cell membrane. Between each pair of flagellar doublets are rows of axonemal dynein ATPases, which power the bending of these organelles, and extending toward the center of the cylinder are radial spokes, which touch upon a central apparatus and regulate axonemal dyneins. This central element consists of two single microtubules, assembled from a unique nucleating site 1 , plus many interconnecting microtubule-associated proteins (reviewed in ref.2). Together they form a structure that provides a cylindrical surface apposing the ends of the radial spokes 3 . mitcheld@upstate.edu, NIH Public Access The nine doublets assemble from a much shorter cylinder of nine triplet microtubules, the basal body or centriole, which is anchored to the cell surface and stabilized in the cytoplasm by other cytoskeletal elements. Basal bodies that anchor flagella are often interchangeable during the cell cycle with centrioles 4 , and these two names should be considered as two functional descriptions for the same structure....

show abstract

The SM19 gene, required for duplication of basal bodies in Paramecium, encodes a novel tubulin, η-tubulin

Cited by 66 publications

References 22 publications

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Evolution and persistence of the cilium

The Evolution of Eukaryotic Cilia and Flagella as Motile and Sensory Organelles

Contact Info

Product

Resources

About