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.

Fig. 1.

Distribution of centriolar and centrosomal proteins among eukaryotes. Protein homologues were identified in 45 eukaryotic genomes, including 29 ciliated species and 16 non-ciliated species (grey). The presence of homologue(s) is indicated by a plus symbol (+). ‘Core’ proteins are conserved ancestral centriolar proteins. ‘Centrosomal’ proteins are associated with centrosomal functions. ‘Pole’ proteins might have fulfilled a function in the ancestral spindle pole. ‘Controls’ are proteins that are associated with general microtubule dynamics. ‘Ancestral’ proteins are present among extant eukaryotes. ‘Holozoan’ proteins have a restricted presence in Holozoa (Metazoa and M. brevicollis). The asterisk indicates sequence drift of core and centrosomal proteins in C. elegans; divergent homologues known in the literature but not identified by our approach are highlighted with a pink border.

Fig. 2.

Distribution of ciliopathy-associated proteins among eukaryotes. Protein homologues were identified in 45 eukaryotic genomes, including 29 ciliated species and 16 non-ciliated species (grey). The presence of homologue(s) is indicated by a plus symbol (+). The proteins are grouped according to the ciliopathy (MKS, BBS and NPHP) or/and ciliary photoreceptor association. ‘Eye-associated’ proteins show a distribution that correlates with ciliary ‘c’ photoreceptors. The light blue shade indicates the exclusive presence of rhabdomeric ‘r’ photoreceptors.