Speculations on the evolution of 9+2 organelles and the role of central pair microtubules

Abstract

Motility generated by 9+2 organelles, variably called cilia or flagella, evolved before divergence from the last common ancestor of extant eukaryotes. In order to understand better how motility in these organelles is regulated, evolutionary steps that led to the present 9+2 morphology are considered. In addition, recent advances in our knowledge of flagellar assembly, together with heightened appreciation of the widespread role of cilia in sensory processes, suggest that these organelles may have served multiple roles in early eukaryotic cells. In addition to their function as undulating motility organelles, we speculate that protocilia were the primary determinants of cell polarity and directed motility in early eukaryotes, and that they provided the first defined membrane domain for localization of receptors that allowed cells to respond tactically to environmental cues. Initially, motility associated with these protocilia may have been gliding motility rather than the more complex bend propagation. Once these protocilia became functional motile organelles for beating, we believe that addition of an asymmetric central apparatus, capable of transducing signals to dynein motors and altering beat parameters, provided refined directional control in response to tactic signals. This paper presents hypothesized steps in this evolutionary process, and examples to support these hypotheses.

Evolution and persistence of the cilium

“…The major difference between our hypothesis and the alternatives discussed above, particularly the hypothesis of de novo differentiation [Cavalier-Smith, 1987;Mitchell, 2004;Jekely and Arendt, 2006], is the account of centriolar origin just given. For the sake of completeness, we sketch our opinion of preconditions in the host cell necessary for morphogenesis of the protocilium and an evolutionary sequence leading to the modern 9 1 2 organelle.…”

“…The second suggestion is de novo differentiation within the proto-eukaryotic cytoplasm, by assembly of cytoplasmic microtubules, which evolved earlier [Cavalier-Smith, 1987;Mitchell, 2004;Jekely and Arendt, 2006]. This hypothesis also provides no explanations for the origin of the centriole as an apparent self-replicating organelle with a fixed symmetry.…”

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

“…As argued in more detail elsewhere, I propose that motility regulation by a central apparatus provided a strong selective advantage to the organism in which it evolved, and that the most successful regulatory mechanism was based on an apparatus built on a scaffold of two central microtubules, with regulatory signals transmitted through radial spokes of a defined length 44,47 . The geometry of this regulatory mechanism presumably favors an outer cylinder of precisely nine doublet microtubules, with the distance between doublets determined by the reach of dyneins that must span each interdoublet gap.…”

“…Alternatively, if substrate adhesion through IFT-associated protoflagellar transmembrane proteins was strong, and cell body adhesion proportionately weak, retrograde IFT could support gliding motility. Flagellar gliding as a means of locomotion is common in many pelagic, benthic and soil flagellates today, and such surface motility has also been described for metazoan cilia, suggesting that it was either an early adaptation of the IFT system, or one that has happened repeatedly during subsequent evolution 44 . As the coupling mechanisms between flagellar adhesion molecules and gliding motors have not been widely studied, their evolutionary history remains unknown.…”

“…In G 1 phase of the cell cycle, prior to DNA and MTOC duplication, the primitive cell would have had a single MTOC, with a single array of microtubules directed away from the nucleus that defined the polarity of the cell. It is this cytoplasmic microtubule array that most likely provided the raw material for evolution of the flagellar axoneme [42][43][44] .…”