One of the Nine Doublet Microtubules of Eukaryotic Flagella Exhibits Unique and Partially Conserved Structures

Jianfeng Lin, Thomas Heuser, Kangkang Song, Xiaofeng Fu, Daniela Nicastro

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

The axonemal core of motile cilia and flagella consists of nine doublet microtubules surrounding two central single microtubules. Attached to the doublets are thousands of dynein motors that produce sliding between neighboring doublets, which in turn causes flagellar bending. Although many structural features of the axoneme have been described, structures that are unique to specific doublets remain largely uncharacterized. These doublet-specific structures introduce asymmetry into the axoneme and are likely important for the spatial control of local microtubule sliding. Here, we used cryo-electron tomography and doublet-specific averaging to determine the 3D structures of individual doublets in the flagella of two evolutionarily distant organisms, the protist Chlamydomonas and the sea urchin Strongylocentrotus. We demonstrate that, in both organisms, one of the nine doublets exhibits unique structural features. Some of these features are highly conserved, such as the inter-doublet link i-SUB5-6, which connects this doublet to its neighbor with a periodicity of 96 nm. We also show that the previously described inter-doublet links attached to this doublet, the o-SUB5-6 in Strongylocentrotus and the proximal 1-2 bridge in Chlamydomonas, are likely not homologous features. The presence of inter-doublet links and reduction of dynein arms indicate that inter-doublet sliding of this unique doublet against its neighbor is limited, providing a rigid plane perpendicular to the flagellar bending plane. These doublet-specific features and the non-sliding nature of these connected doublets suggest a structural basis for the asymmetric distribution of dynein activity and inter-doublet sliding, resulting in quasi-planar waveforms typical of 9+2 cilia and flagella.

Original languageEnglish (US)
Article numbere46494
JournalPLoS One
Volume7
Issue number10
DOIs
StatePublished - Oct 10 2012

Fingerprint

Dyneins
Flagella
Strongylocentrotus
flagellum
Microtubules
microtubules
Axoneme
Chlamydomonas
Cilia
cilia
Electron Microscope Tomography
Sea Urchins
tomography
organisms
Periodicity
Echinoidea
periodicity
Tomography
electrons
Electrons

ASJC Scopus subject areas

  • Medicine(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

One of the Nine Doublet Microtubules of Eukaryotic Flagella Exhibits Unique and Partially Conserved Structures. / Lin, Jianfeng; Heuser, Thomas; Song, Kangkang; Fu, Xiaofeng; Nicastro, Daniela.

In: PLoS One, Vol. 7, No. 10, e46494, 10.10.2012.

Research output: Contribution to journalArticle

Lin, Jianfeng ; Heuser, Thomas ; Song, Kangkang ; Fu, Xiaofeng ; Nicastro, Daniela. / One of the Nine Doublet Microtubules of Eukaryotic Flagella Exhibits Unique and Partially Conserved Structures. In: PLoS One. 2012 ; Vol. 7, No. 10.
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