Conservation of ciliary proteins in plants with no cilia

Abstract

BackgroundEukaryotic cilia are complex, highly conserved microtubule-based organelles with a broad phylogenetic distribution. Cilia were present in the last eukaryotic common ancestor and many proteins involved in cilia function have been conserved through eukaryotic diversification. However, cilia have also been lost multiple times in different lineages, with at least two losses occurring within the land plants. Whereas all non-seed plants produce cilia for motility of male gametes, some gymnosperms and all angiosperms lack cilia. During these evolutionary losses, proteins with ancestral ciliary functions may be lost or co-opted into different functions.ResultsHere we identify a core set of proteins with an inferred ciliary function that are conserved in ciliated eukaryotic species. We interrogate this genomic dataset to identify proteins with a predicted ancestral ciliary role that have been maintained in non-ciliated land plants. In support of our prediction, we demonstrate that several of these proteins have a flagellar localisation in protozoan trypanosomes. The phylogenetic distribution of these genes within the land plants indicates evolutionary scenarios of either sub- or neo-functionalisation and expression data analysis shows that these genes are highly expressed in Arabidopsis thaliana pollen cells.ConclusionsA large number of proteins possess a phylogenetic ciliary profile indicative of ciliary function. Remarkably, many genes with an ancestral ciliary role are maintained in non-ciliated land plants. These proteins have been co-opted to perform novel functions, most likely before the loss of cilia, some of which appear related to the formation of the male gametes.

Eukaryotic Flagella: Variations in Form, Function, and Composition during Evolution

“…1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 Merchant et al 2007). In contrast, using the same pipeline as for their identification of 'ciliary profile' proteins in land plants, Hodges et al (2011) predict that the number of 'flagellar' proteins in fungi, at least, will be lower than in aflagellate land plants.…”

FOR20, a conserved centrosomal protein, is required for assembly of the transition zone and basal body docking at the cell surface

“…Several other proteins involved in centriolar and ciliary functions are conserved in acentriolar plants (Laligné et al, 2010;Hodges et al, 2011). Many of them have, or are supposed to have, a role in cytoskeletal/microtubule organisation (Gardiner and Marc, 2011;Hodges et al, 2011) suggesting that they are maintained for microtubular organisation in non-ciliated plants (Hodges et al, 2011).…”

“…Many of them have, or are supposed to have, a role in cytoskeletal/microtubule organisation (Gardiner and Marc, 2011;Hodges et al, 2011) suggesting that they are maintained for microtubular organisation in non-ciliated plants (Hodges et al, 2011). The member of the centrosomal FOP family conserved in land plants, TONNEAU1, is known to interact with centrin and to be required for correct assembly of the preprophase band (Azimzadeh et al, 2008).…”

The conserved ciliary protein Bug22 controls planar beating ofChlamydomonasflagella

“…This protein is highly conserved in ciliated organisms as well as in higher plants (Hodges et al, 2011;Laligné et al, 2010). Alignment of Bug22 with its human ortholog (GenBank NP_037374.1) showed 89% identity within 98% coverage.…”

“…Alignment of Bug22 with its human ortholog (GenBank NP_037374.1) showed 89% identity within 98% coverage. Bug22 has been shown to be a flagellar protein in Paramecium and Trypanosome (Hodges et al, 2011;Laligné et al, 2010). Immunogold labeling of Bug22 in Paramecium shows that it is preferentially localized between ciliary membrane and axoneme, as well as to basal bodies.…”