Six subgroups and extensive recent duplications characterize the evolution of the eukaryotic tubulin protein family

Genome Biology and Evolution

Volumn 6, Issue 9, 2014, Pages 2274-2288

  Findeisen, Peggy ^a   Mühlhausen, Stefanie ^a   Dempewolf, Silke ^a   Hertzog, Jonny ^a   Zietlow, Alexander ^a   Carlomagno, Teresa ^b   Kollmar, Martin ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Artubulin; Eukaryotic evolution; FtsZ; Gene duplication; Tubulin; TubZ

Indexed keywords

TUBULIN;

AMINO ACID SEQUENCE; ANIMAL; ARCHAEON; BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; EUKARYOTE; GENE DUPLICATION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY;

AMINO ACID SEQUENCE; ANIMALS; ARCHAEA; BACTERIA; EUKARYOTA; EVOLUTION, MOLECULAR; GENE DUPLICATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; TUBULIN;

EID: 84930359427     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu187     Document Type: Article

References (65)

1. Adl SM, et al. 2012. The revised classification of eukaryotes. J Eukaryot Microbiol. 59:429-493.
2. Aylett CHS, Löwe J, Amos LA. 2011. New insights into the mechanisms of cytomotive actin and tubulin filaments. Int Rev Cell Mol Biol. 292:1-71.
3. Aylett CHS, Wang Q, Michie KA, Amos LA, Löwe J. 2010. Filament structure of bacterial tubulin homologue TubZ. Proc Natl Acad Sci USA. 107:19766-19771.
4. Breviario D, Gianì S, Morello L. 2013. Multiple tubulins: evolutionary aspects and biological implications. Plant J Cell Mol Biol. 75:202-218.
5. Brown MW, Spiegel FW, Silberman JD. 2009. Phylogeny of the "forgotten" cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol. 26:2699-2709.
6. Campanella JJ, Bitincka L, Smalley J. 2003. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:29.
7. Chenna R, et al. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-500.
8. Darriba D, Taboada GL, Doallo R, Posada D. 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164-1165.
9. Dutcher SK. 2003. Long-lost relatives reappear: identification of new members of the tubulin superfamily. Curr Opin Microbiol. 6:634-640.
10. Dyer N. 2009. Tubulin and its prokaryotic homologue FtsZ: a structural and functional comparison. Sci Prog. 92:113-137.
11. Eckert C, Hammesfahr B, Kollmar M. 2011. A holistic phylogeny of the coronin gene family reveals an ancient origin of the tandem-coronin, defines a new subfamily, and predicts protein function. BMC Evol Biol. 11:268.
12. Elsik CG, et al. 2009. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522-528.
13. Fulton C, Simpson PA. 1976. Selective synthesis and utilisation of flagellar tubulin. The multi-tubulin hypothesis. In: Goldman R, Pollard T, Rosenbaum J, editors. Cell motility, Vol. 3. New York: Cold Spring Harbor Laboratory Press. p. 987-1005.
14. Garreau De Loubresse N, Ruiz F, Beisson J, Klotz C. 2001. Role of deltatubulin and the C-tubule in assembly of Paramecium basal bodies. BMC Cell Biol. 2:4.
15. Gong Y, et al. 2010. Alpha-tubulin and small subunit rRNA phylogenies of peritrichs are congruent and do not support the clustering of mobilids and sessilids (Ciliophora, Oligohymenophorea). J Eukaryot Microbiol. 57:265-272.
16. Hampl V, et al. 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc Natl Acad Sci USA. 106:3859-3864.
17. Hatje K, Hammesfahr B, Kollmar M. 2013. WebScipio: reconstructing alternative splice variants of eukaryotic proteins. Nucleic Acids Res. 41:W504-W509.
18. Hatje K, Kollmar M. 2013. Expansion of the mutually exclusive spliced exome in Drosophila. Nat Commun. 4:2460.
19. Hatje K, et al. 2011. Cross-species protein sequence and gene structure prediction with fine-tuned Webscipio 2.0 and Scipio. BMC Res Notes. 4:265.
20. He D, et al. 2014. An alternative root for the eukaryote tree of life. Curr Biol. 24:465-470.
21. Huang K-H, Durand-Heredia J, Janakiraman A. 2013. FtsZ ring stability: of bundles, tubules, crosslinks, and curves. J Bacteriol. 195:1859-1868.
22. Jackson AP, Vaughan S, Gull K. 2006. Evolution of tubulin gene arrays in Trypanosomatid parasites: genomic restructuring in Leishmania. BMC Genomics 7:261.
23. Jenkins C, et al. 2002. Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc Natl Acad Sci USA. 99:17049-17054.
24. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
25. Keeling PJ. 2009. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol. 56:1-8.
26. Khodiyar VK, et al. 2007. A revised nomenclature for the human and rodent a-tubulin gene family. Genomics 90:285-289.
27. Kin T, Ono Y. 2007. Idiographica: a general-purpose web application to build idiograms on-demand for human, mouse and rat. Bioinformatics 23:2945-2946.
28. Kollmar M, Lbik D, Enge S. 2012. Evolution of the eukaryotic ARP2/3 activators of the WASP family: WASP, WAVE, WASH, and WHAMM, and the proposed new family members WAWH and WAML. BMC Res Notes. 5:88.
29. Kurtzman CP. 2011. Phylogeny of the ascomycetous yeasts and the renaming of Pichia anomala to Wickerhamomyces anomalus. Antonie Van Leeuwenhoek. 99:13-23.
30. Larsen RA, et al. 2007. Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev. 21:1340-1352.
31. Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658-1659.
32. Libusová L, Dráber P. 2006. Multiple tubulin forms in ciliated protozoan Tetrahymena and Paramecium species. Protoplasma 227:65-76.
33. Martin-Galiano AJ, et al. 2011. Bacterial tubulin distinct loop sequences and primitive assembly properties support its origin from a eukaryotic tubulin ancestor. J Biol Chem. 286:19789-19803.
34. Mühlhausen S, Kollmar M. 2013. Whole genome duplication events in plant evolution reconstructed and predicted using myosin motor proteins. BMC Evol Biol. 13:202.
35. Nawrotek A, Knossow M, Gigant B. 2011. The determinants that govern microtubule assembly from the atomic structure of GTP-tubulin. J Mol Biol. 412:35-42.
36. Nielsen MG, Gadagkar SR, Gutzwiller L. 2010. Tubulin evolution in insects: gene duplication and subfunctionalization provide specialized isoforms in a functionally constrained gene family. BMC Evol Biol. 10:113.
37. Nogales E. 2001. Structural insight into microtubule function. Annu Rev Biophys Biomol Struct. 30:397-420.
38. Nozaki H, et al. 2009. Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Mol Phylogenet Evol. 53:872-880.
39. Oakley BR. 2000. An abundance of tubulins. Trends Cell Biol. 10:537-542.
40. Odronitz F, Becker S, Kollmar M. 2009. Reconstructing the phylogeny of 21 completely sequenced arthropod species based on their motor proteins. BMC Genomics 10:173.
41. Odronitz F, Kollmar M. 2006. Pfarao: a web application for protein family analysis customized for cytoskeletal and motor proteins (CyMoBase). BMC Genomics 7:300.
42. Odronitz F, Kollmar M. 2007. Drawing the tree of eukaryotic life based on the analysis of 2, 269 manually annotated myosins from 328 species. Genome Biol. 8:R196.
43. Ohno S. 1970. Evolution by gene duplication. New York: Springer-Verlag.
44. Parfrey LW, et al. 2010. Broadly sampled multigene analyses yield a wellresolved eukaryotic tree of life. Syst Biol. 59:518-533.
45. Pilhofer M, Ladinsky MS, McDowall AW, Petroni G, Jensen GJ. 2011. Microtubules in bacteria: ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol. 9:e1001213.
46. Pillmann H, Hatje K, Odronitz F, Hammesfahr B, Kollmar M. 2011. Predicting mutually exclusive spliced exons based on exon length, splice site and reading frame conservation, and exon sequence homology. BMC Bioinformatics 12:270.
47. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490.
48. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
49. Ross I, Clarissa C, Giddings TH Jr, Winey M. 2013. "-tubulin is essential in Tetrahymena thermophila for the assembly and stability of basal bodies. J Cell Sci. 126:3441-3451.
50. Schlieper D, Oliva MA, Andreu JM, Löwe J. 2005. Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci USA. 102:9170-9175.
51. Simpson AGB, Inagaki Y, Roger AJ. 2006. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. Mol Biol Evol. 23:615-625.
52. Sontag CA, Sage H, Erickson HP. 2009. BtubA-BtubB heterodimer is an essential intermediate in protofilament assembly. PLoS One 4:e7253.
53. Stanke M, Morgenstern B. 2005. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33:W465-W467.
54. Steinke D, Hoegg S, Brinkmann H, Meyer A. 2006. Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol. 4:16.
55. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 56:564-577.
56. Van De Peer Y, Maere S, Meyer A. 2010. 2R or not 2R is not the question anymore. Nat Rev Genet. 11:166.
57. Vaughan S, et al. 2000. New tubulins in protozoal parasites. Curr Biol. 10:R258-R259.
58. Wägele JW, Bartolomaeus T. 2014. Deep metazoan phylogeny: the backbone of the tree of life, new insights from analyses of molecules, morphology, and theory of data analysis. Berlin (Germany): De Gruyter [cited 2014 Aug. 18] Available from: http://www.degruyter.com/view/product/181254.
59. Walker DM, Castlebury LA, Rossman AY, White JF. 2012. New molecular markers for fungal phylogenetics: two genes for species-level systematics in the Sordariomycetes (Ascomycota). Mol Phylogenet Evol. 64:500-512.
60. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691-699.
61. Wickstead B, Gull K. 2011. The evolution of the cytoskeleton. J Cell Biol. 194:513-525.
62. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713.
63. Yi Z, Katz LA, Song W. 2012. Assessing whether alpha-tubulin sequences are suitable for phylogenetic reconstruction of Ciliophora with insights into its evolution in euplotids. PloS One 7:e40635.
64. Yutin N, Koonin EV. 2012. Archaeal origin of tubulin. Biol Direct. 7:10.
65. Zimin AV, et al. 2009. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 10:R42.