Speculations on the evolution of 9+2 organelles and the role of central pair microtubules - PubMed (original) (raw)
Review
Speculations on the evolution of 9+2 organelles and the role of central pair microtubules
David R Mitchell. Biol Cell. 2004 Dec.
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.
Figures
Figure 1
Diagrams of proposed stages in evolution of 9+2 cilia and flagella. (A) A centrosome nucleates microtubules bidirectionally, toward and away from the nucleus. (B) Lengthening microtubules that radiate away from the nucleus generate a polarized cell. Addition of membrane-associated microtubule motors allows gliding motility. (C) Sliding motors between parallel microtubules leads to vibrating/undulating motility, and necessitates stabilization through additional links between the centrosome and the membrane, defining two membrane domains (cell body and flagellum). (D) Formation of doublets and addition of the radial spoke-central and pair apparatus allow complex regulation of undulating motility, including receptor-dependent tactic responses. Rotation of a twisted central pair promotes effective interaction of specific central pair projections with radial spokes to control dyneins. (A–C) modified from Cavalier-Smith (1982), (D) modified from Mitchell (2003b).
Similar articles
- The evolution of eukaryotic cilia and flagella as motile and sensory organelles.
Mitchell DR. Mitchell DR. Adv Exp Med Biol. 2007;607:130-40. doi: 10.1007/978-0-387-74021-8_11. Adv Exp Med Biol. 2007. PMID: 17977465 Free PMC article. Review. - Assembly, Functions and Evolution of Archaella, Flagella and Cilia.
Khan S, Scholey JM. Khan S, et al. Curr Biol. 2018 Mar 19;28(6):R278-R292. doi: 10.1016/j.cub.2018.01.085. Curr Biol. 2018. PMID: 29558648 Review. - Radial Spokes-A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella.
Zhu X, Liu Y, Yang P. Zhu X, et al. Cold Spring Harb Perspect Biol. 2017 May 1;9(5):a028126. doi: 10.1101/cshperspect.a028126. Cold Spring Harb Perspect Biol. 2017. PMID: 27940518 Free PMC article. Review. - Early evolution of microtubules and undulipodia.
Szathmáry E. Szathmáry E. Biosystems. 1987;20(2):115-31. doi: 10.1016/0303-2647(87)90039-6. Biosystems. 1987. PMID: 3300813 Review. - Microtubule-depolymerizing kinesins in the regulation of assembly, disassembly, and length of cilia and flagella.
Hu Z, Liang Y, Meng D, Wang L, Pan J. Hu Z, et al. Int Rev Cell Mol Biol. 2015;317:241-65. doi: 10.1016/bs.ircmb.2015.01.008. Epub 2015 Mar 5. Int Rev Cell Mol Biol. 2015. PMID: 26008787 Review.
Cited by
- Cerebral furin deficiency causes hydrocephalus in mice.
Xie S, Xie X, Tang J, Luo B, Chen J, Wen Q, Zhou J, Chen G. Xie S, et al. Genes Dis. 2023 Jul 8;11(3):101009. doi: 10.1016/j.gendis.2023.04.037. eCollection 2024 May. Genes Dis. 2023. PMID: 38292192 Free PMC article. - Three-dimensional flagella structures from animals' closest unicellular relatives, the Choanoflagellates.
Pinskey JM, Lagisetty A, Gui L, Phan N, Reetz E, Tavakoli A, Fu G, Nicastro D. Pinskey JM, et al. Elife. 2022 Nov 17;11:e78133. doi: 10.7554/eLife.78133. Elife. 2022. PMID: 36384644 Free PMC article. - Cryo-EM structure of an active central apparatus.
Han L, Rao Q, Yang R, Wang Y, Chai P, Xiong Y, Zhang K. Han L, et al. Nat Struct Mol Biol. 2022 May;29(5):472-482. doi: 10.1038/s41594-022-00769-9. Epub 2022 May 16. Nat Struct Mol Biol. 2022. PMID: 35578022 Free PMC article. - Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota.
Galindo LJ, López-García P, Torruella G, Karpov S, Moreira D. Galindo LJ, et al. Nat Commun. 2021 Aug 17;12(1):4973. doi: 10.1038/s41467-021-25308-w. Nat Commun. 2021. PMID: 34404788 Free PMC article. - Expansion microscopy provides new insights into the cytoskeleton of malaria parasites including the conservation of a conoid.
Bertiaux E, Balestra AC, Bournonville L, Louvel V, Maco B, Soldati-Favre D, Brochet M, Guichard P, Hamel V. Bertiaux E, et al. PLoS Biol. 2021 Mar 11;19(3):e3001020. doi: 10.1371/journal.pbio.3001020. eCollection 2021 Mar. PLoS Biol. 2021. PMID: 33705377 Free PMC article.
References
- Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, Zuker CS. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell. 2004;117:527–539. - PubMed
- Baccetti B. Evolutionary trends in sperm structure. Comp Biochem Physiol A. 1986;85:29–36. - PubMed
- Baccetti B, Burrini AG, Dallai R, Pallini V. A motile system of singlet microtubules in spermatozoa. Cell Motility. 1982;2:93–101.
- Bloodgood RA. Direct visualization of of dynamic membrane events in cilia. J Exp Zool. 1980;213:293–295.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources