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, 17 (4), 1734-43

A "Holistic" Kinesin Phylogeny Reveals New Kinesin Families and Predicts Protein Functions

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A "Holistic" Kinesin Phylogeny Reveals New Kinesin Families and Predicts Protein Functions

Bill Wickstead et al. Mol Biol Cell.

Abstract

Kinesin superfamily proteins are ubiquitous to all eukaryotes and essential for several key cellular processes. With the establishment of genome sequence data for a substantial number of eukaryotes, it is now possible for the first time to analyze the complete kinesin repertoires of a diversity of organisms from most eukaryotic kingdoms. Such a "holistic" approach using 486 kinesin-like sequences from 19 eukaryotes and analyzed by Bayesian techniques, identifies three new kinesin families, two new phylum-specific groups, and unites two previously identified families. The paralogue distribution suggests that the eukaryotic cenancestor possessed nearly all kinesin families. However, multiple losses in individual lineages mean that no family is ubiquitous to all organisms and that the present day distribution reflects common biology more than it does common ancestry. In particular, the distribution of four families--Kinesin-2, -9, and the proposed new families Kinesin-16 and -17--correlates with the possession of cilia/flagella, and this can be used to predict a flagellar function for two new kinesin families. Finally, we present a set of hidden Markov models that can reliably place most new kinesin sequences into families, even when from an organism at a great evolutionary distance from those in the analysis.

Figures

Figure 1.
Figure 1.
The “quality” of the kinesin motor domains in a data set of 459 nonredundant kinesin-like proteins (468 211 aa) from 19 diverse organisms as assessed by the hit to Pfam motor domain profile PF00225 (see Materials and Methods). Sequences passing the threshold, e < 10–70, are in black. The positions of four divergent kinesins from well-studied models are shown for information.
Figure 2.
Figure 2.
A Bayesian kinesin motor domain phylogeny encompassing 400 nonredundant sequences from 19 diverse organisms with complete or near-complete genome sequence (see Materials and Methods for details). The tree is arbitrarily rooted using ScSmy1. Prefixes are as follows: At, A. thaliana; Ce, C. elegans; Cm, C. merolae; Cp, C. parvum; Cr, C. reinhardtii; Dd, D. discoideum; Dm, D. melanogaster; Ec, E. cuniculi; Eh, E. histolytica; Gl, G. lamblia; Hs, H. sapiens; Lm, L. major; Pf, P. falciparum; Sc, S. cerevisiae; Sp, S. pombe; Ta, T. annulata; Tb, T. brucei; Tp, T. pseudonana; and Tt, T. thermophila. Nodes that were also found in a majority of 10 Bayesian partial replicates are indicated (thick lines). Support for the inferred topology from 500 neighbor-joining bootstrap replicates is indicated: >50% (empty circles); >75% (filled circles). For clarity, bootstrap values for some higher nodes are omitted, but in all cases the deepest node in any family with >50% support is indicated. Family annotation: family described by standard kinesin nomenclature (dark blue bracket), subfamily (light blue bracket), new kinesin family (solid orange bracket), and new phylum-specific group (dotted orange bracket). Sequences within these groups are emboldened. We find no consensus for monophyly of the proposed families Kinesin-15 and -16 (previously described Kinesin-12 family; asterisks). Predictive HMMs: sequences from Tetrahymena (Tt) are highlighted green or red on the basis of passing or failing the HMM threshold for their respective families (see text for details).
Figure 3.
Figure 3.
Distribution of kinesin families among eukaryotes. (A) Cladogram showing the probable evolutionary relationships of the 19 organisms analyzed. (B) Taxonomic distribution of kinesin families: presence of paralogue (dark blue dot), absence of a paralogue from an incomplete genome (light blue dot), and absence from a complete genome (open dot). Subfamilies are represented by smaller dots. Kinesin families with a proposed role in cilia/flagella are indicated (triangle), as are organisms that build cilia/flagella (square). (C) Consensus of the 10 most parsimonious trees accounting for the observed kinesin paralogue distribution using family presence/absence as a binary character. See legend to Figure 2 for organism abbreviations.
Figure 4.
Figure 4.
Performance of Kinesin-1 and -2 profiles against the data set of 459 nonredundant kinesin-like proteins. The performance of the other HMMs is similar. Sequences used in the HMM seed alignment are in black. TCs and NCs are illustrated.

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