Reconstructing the evolutionary history of the centriole from protein components.
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.
Hodges
Matthew E
ME
Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford OX1 3RE, UK.
Scheumann
Nicole
N
Wickstead
Bill
B
Langdale
Jane A
JA
Gull
Keith
K
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
D011506:Proteins; D014404:Tubulin; D010770:Phosphotransferases
Arthropod Struct Dev. 2006 Dec;35(4):211-30
18089072
Annu Rev Genomics Hum Genet. 2006;7:125-48
16722803
Cell. 2007 Jun 15;129(6):1201-13
17574030
Curr Biol. 2009 Jun 23;19(12):R472-3
19549489
Cell. 2003 Feb 21;112(4):575-87
12600319
Methods Enzymol. 1982;81:17-25
7098862
Nat Cell Biol. 2000 Jan;2(1):30-5
10620804
Curr Biol. 2005 Dec 20;15(24):2199-207
16326102
J Cell Biol. 2007 Sep 10;178(6):905-12
17785518
Am J Hum Genet. 2007 Jan;80(1):1-11
17160889
J Cell Sci. 2004 Apr 1;117(Pt 9):1619-30
15075224
Science. 2006 Aug 4;313(5787):629-33
16888132
Gene. 2009 Aug 1;442(1-2):63-72
19393304
Mol Biol Cell. 2007 Apr;18(4):1293-301
17267688
Curr Biol. 2009 Jun 23;19(12):1005-11
19481458
Z Zellforsch Mikrosk Anat. 1969;96(1):63-5
4890664
Curr Biol. 2007 Sep 4;17(17):1465-72
17689959
Dev Cell. 2008 Dec;15(6):901-12
19081077
Nature. 2009 Feb 12;457(7231):818-23
19212399
J Cell Sci. 2003 Jul 1;116(Pt 13):2635-46
12746491
Mol Biol Cell. 1998 Jun;9(6):1293-308
9614175
J Cell Biol. 1974 Oct;63(1):325-9
4424205
Int J Dev Biol. 2003;47(7-8):563-71
14756332
Curr Biol. 2004 May 25;14(10):863-73
15186742
J Neurochem. 2007 Apr;101(1):274-88
17394468
Eukaryot Cell. 2005 Jul;4(7):1253-63
16002651
Dev Cell. 2003 Mar;4(3):431-9
12636923
J Cell Biol. 2002 Sep 30;158(7):1183-93
12356863
Science. 2007 Oct 12;318(5848):245-50
17932292
PLoS One. 2008;3(11):e3778
19020665
Cell. 2001 May 18;105(4):547-58
11371350
Curr Opin Cell Biol. 2003 Feb;15(1):96-104
12517710
Dev Biol. 1986 Oct;117(2):456-87
2428682
Dev Cell. 2004 Dec;7(6):815-29
15572125
Curr Biol. 2009 Jun 23;19(12):1012-8
19481460
Nat Cell Biol. 2005 Feb;7(2):115-25
15665853
Syst Biol. 2003 Oct;52(5):696-704
14530136
Adv Parasitol. 1976;14:195-265
769503
Exp Cell Res. 1997 Jul 10;234(1):183-90
9223385
Adv Exp Med Biol. 2007;607:119-29
17977464
Curr Biol. 2007 Dec 18;17(24):2169-74
18082404
Science. 2005 Jul 15;309(5733):416-22
16020726
PLoS One. 2007 Aug 15;2(8):e749
17710148
Bioinformatics. 2003 Aug 12;19(12):1572-4
12912839
Science. 2004 Oct 29;306(5697):869-71
15514158
Nature. 2006 Nov 30;444(7119):619-23
17136092
J Cell Sci. 2007 Jan 1;120(Pt 1):7-15
17182899
J Cell Sci. 2006 Jun 15;119(Pt 12):2405-13
16720646
Dis Aquat Organ. 2005 Dec 30;68(1):51-63
16465834
Traffic. 2007 Dec;8(12):1708-1721
17897317
Philos Trans R Soc Lond B Biol Sci. 2001 Oct 29;356(1414):1545-63
11604122
Int J Biol Sci. 2006;2(3):142-8
16763674
Nat Cell Biol. 2005 Nov;7(11):1140-6
16244668
Curr Biol. 2002 Aug 6;12(15):1287-92
12176356
Nat Cell Biol. 2009 Jul;11(7):825-31
19503075
Proc R Soc Lond B Biol Sci. 1978 Jun 5;201(1145):375-99
27809
Dev Cell. 2004 Apr;6(4):511-23
15068791
J Mol Biol. 1990 Oct 5;215(3):403-10
2231712