title: Reconstructing the evolutionary history of the centriole from protein components.
abstract: Centrioles are highly conserved structures that fulfil important cellular functions, such as nucleation of cilia and flagella (basal-body function) and organisation of pericentriolar material to form the centrosome. The evolution of these functions can be inferred from the distribution of the molecular components of extant centrioles and centrosomes. Here, we undertake an evolutionary analysis of 53 proteins known either for centriolar association or for involvement in cilia-associated pathologies. By linking protein distribution in 45 diverse eukaryotes with organism biology, we provide molecular evidence to show that basal-body function is ancestral, whereas the presence of the centrosome is specific to the Holozoa. We define an ancestral centriolar inventory of 14 core proteins, Polo-like-kinase, and proteins associated with Bardet-Biedl syndrome (BBS) and Meckel-Gruber syndrome. We show that the BBSome is absent from organisms that produce cilia only for motility, predicting a dominant and ancient role for this complex in sensory function. We also show that the unusual centriole of Caenorhabditis elegans is highly divergent in both protein composition and sequence. Finally, we demonstrate a correlation between the presence of specific centriolar proteins and eye evolution. This correlation is used to predict proteins with functions in the development of ciliary, but not rhabdomeric, eyes.
authors.affiliation: Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford OX1 3RE, UK.
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Hodges
authors.forename: Nicole
authors.initials: N
authors.lastname: Scheumann
authors.forename: Bill
authors.initials: B
authors.lastname: Wickstead
authors.forename: Jane A
authors.initials: JA
authors.lastname: Langdale
authors.forename: Keith
authors.initials: K
authors.lastname: Gull
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000378:metabolism; D002502:Centrioles / Q000737:chemistry* / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D002923:Cilia / Q000378:metabolism; D005057:Eukaryotic Cells / Q000378:metabolism; D019143:Evolution, Molecular; D006801:Humans; D010770:Phosphotransferases / Q000378:metabolism; D010802:Phylogeny; D011506:Proteins / Q000378:metabolism*; D014404:Tubulin / Q000235:genetics
chemical_list: D011506:Proteins; D014404:Tubulin; D010770:Phosphotransferases
references.citation: Arthropod Struct Dev. 2006 Dec;35(4):211-30
references.pmid: 18089072
references.citation: Annu Rev Genomics Hum Genet. 2006;7:125-48
references.pmid: 16722803
references.citation: Cell. 2007 Jun 15;129(6):1201-13
references.pmid: 17574030
references.citation: Curr Biol. 2009 Jun 23;19(12):R472-3
references.pmid: 19549489
references.citation: Cell. 2003 Feb 21;112(4):575-87
references.pmid: 12600319
references.citation: Methods Enzymol. 1982;81:17-25
references.pmid: 7098862
references.citation: Nat Cell Biol. 2000 Jan;2(1):30-5
references.pmid: 10620804
references.citation: Curr Biol. 2005 Dec 20;15(24):2199-207
references.pmid: 16326102
references.citation: J Cell Biol. 2007 Sep 10;178(6):905-12
references.pmid: 17785518
references.citation: Am J Hum Genet. 2007 Jan;80(1):1-11
references.pmid: 17160889
references.citation: J Cell Sci. 2004 Apr 1;117(Pt 9):1619-30
references.pmid: 15075224
references.citation: Science. 2006 Aug 4;313(5787):629-33
references.pmid: 16888132
references.citation: Gene. 2009 Aug 1;442(1-2):63-72
references.pmid: 19393304
references.citation: Mol Biol Cell. 2007 Apr;18(4):1293-301
references.pmid: 17267688
references.citation: Curr Biol. 2009 Jun 23;19(12):1005-11
references.pmid: 19481458
references.citation: Z Zellforsch Mikrosk Anat. 1969;96(1):63-5
references.pmid: 4890664
references.citation: Curr Biol. 2007 Sep 4;17(17):1465-72
references.pmid: 17689959
references.citation: Dev Cell. 2008 Dec;15(6):901-12
references.pmid: 19081077
references.citation: Nature. 2009 Feb 12;457(7231):818-23
references.pmid: 19212399
references.citation: J Cell Sci. 2003 Jul 1;116(Pt 13):2635-46
references.pmid: 12746491
references.citation: Mol Biol Cell. 1998 Jun;9(6):1293-308
references.pmid: 9614175
references.citation: J Cell Biol. 1974 Oct;63(1):325-9
references.pmid: 4424205
references.citation: Int J Dev Biol. 2003;47(7-8):563-71
references.pmid: 14756332
references.citation: Curr Biol. 2004 May 25;14(10):863-73
references.pmid: 15186742
references.citation: J Neurochem. 2007 Apr;101(1):274-88
references.pmid: 17394468
references.citation: Eukaryot Cell. 2005 Jul;4(7):1253-63
references.pmid: 16002651
references.citation: Dev Cell. 2003 Mar;4(3):431-9
references.pmid: 12636923
references.citation: J Cell Biol. 2002 Sep 30;158(7):1183-93
references.pmid: 12356863
references.citation: Science. 2007 Oct 12;318(5848):245-50
references.pmid: 17932292
references.citation: PLoS One. 2008;3(11):e3778
references.pmid: 19020665
references.citation: Cell. 2001 May 18;105(4):547-58
references.pmid: 11371350
references.citation: Curr Opin Cell Biol. 2003 Feb;15(1):96-104
references.pmid: 12517710
references.citation: Dev Biol. 1986 Oct;117(2):456-87
references.pmid: 2428682
references.citation: Dev Cell. 2004 Dec;7(6):815-29
references.pmid: 15572125
references.citation: Curr Biol. 2009 Jun 23;19(12):1012-8
references.pmid: 19481460
references.citation: Nat Cell Biol. 2005 Feb;7(2):115-25
references.pmid: 15665853
references.citation: Syst Biol. 2003 Oct;52(5):696-704
references.pmid: 14530136
references.citation: Adv Parasitol. 1976;14:195-265
references.pmid: 769503
references.citation: Exp Cell Res. 1997 Jul 10;234(1):183-90
references.pmid: 9223385
references.citation: Adv Exp Med Biol. 2007;607:119-29
references.pmid: 17977464
references.citation: Curr Biol. 2007 Dec 18;17(24):2169-74
references.pmid: 18082404
references.citation: Science. 2005 Jul 15;309(5733):416-22
references.pmid: 16020726
references.citation: PLoS One. 2007 Aug 15;2(8):e749
references.pmid: 17710148
references.citation: Bioinformatics. 2003 Aug 12;19(12):1572-4
references.pmid: 12912839
references.citation: Science. 2004 Oct 29;306(5697):869-71
references.pmid: 15514158
references.citation: Nature. 2006 Nov 30;444(7119):619-23
references.pmid: 17136092
references.citation: J Cell Sci. 2007 Jan 1;120(Pt 1):7-15
references.pmid: 17182899
references.citation: J Cell Sci. 2006 Jun 15;119(Pt 12):2405-13
references.pmid: 16720646
references.citation: Dis Aquat Organ. 2005 Dec 30;68(1):51-63
references.pmid: 16465834
references.citation: Traffic. 2007 Dec;8(12):1708-1721
references.pmid: 17897317
references.citation: Philos Trans R Soc Lond B Biol Sci. 2001 Oct 29;356(1414):1545-63
references.pmid: 11604122
references.citation: Int J Biol Sci. 2006;2(3):142-8
references.pmid: 16763674
references.citation: Nat Cell Biol. 2005 Nov;7(11):1140-6
references.pmid: 16244668
references.citation: Curr Biol. 2002 Aug 6;12(15):1287-92
references.pmid: 12176356
references.citation: Nat Cell Biol. 2009 Jul;11(7):825-31
references.pmid: 19503075
references.citation: Proc R Soc Lond B Biol Sci. 1978 Jun 5;201(1145):375-99
references.pmid: 27809
references.citation: Dev Cell. 2004 Apr;6(4):511-23
references.pmid: 15068791
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712