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First published online June 10, 2005; 10.1104/pp.105.060913 Plant Physiology 138:1711-1722 (2005) © 2005 American Society of Plant Biologists Origin and Evolution of Kinesin-Like Calmodulin-Binding Protein1,[w]Department of Biology, Colorado State University, Fort Collins, Colorado 80523
Kinesin-like calmodulin-binding protein (KCBP), a member of the Kinesin-14 family, is a C-terminal microtubule motor with three unique domains including a myosin tail homology region 4 (MyTH4), a talin-like domain, and a calmodulin-binding domain (CBD). The MyTH4 and talin-like domains (found in some myosins) are not found in other reported kinesins. A calmodulin-binding kinesin called kinesin-C (SpKinC) isolated from sea urchin (Strongylocentrotus purpuratus) is the only reported kinesin with a CBD. Analysis of the completed genomes of Homo sapiens, Saccharomyces cerevisiae, Caenorhabditis elegans, Drosophila melanogaster, and a red alga (Cyanidioschyzon merolae 10D) did not reveal the presence of a KCBP. This prompted us to look at the origin of KCBP and its relationship to SpKinC. To address this, we isolated KCBP from a gymnosperm, Picea abies, and a green alga, Stichococcus bacillaris. In addition, database searches resulted in identification of KCBP in another green alga, Chlamydomonas reinhardtii, and several flowering plants. Gene tree analysis revealed that the motor domain of KCBPs belongs to a clade within the Kinesin-14 (C-terminal motors) family. Only land plants and green algae have a kinesin with the MyTH4 and talin-like domains of KCBP. Further, our analysis indicates that KCBP is highly conserved in green algae and land plants. SpKinC from sea urchin, which has the motor domain similar to KCBP and contains a CBD, lacks the MyTH4 and talin-like regions. Our analysis indicates that the KCBPs, SpKinC, and a subset of the kinesin-like proteins are all more closely related to one another than they are to any other kinesins, but that either KCBP gained the MyTH4 and talin-like domains or SpKinC lost them.
Members of the kinesin superfamily of microtubule (MT) motor proteins have been identified in many taxa ranging from protists to plants and animals (Reddy and Day, 2001  ; Vale, 2003). The members of the kinesin superfamily have a highly conserved motor domain with ATP- and MT-binding sites. In addition, most kinesins have a less conserved coiled-coil region that is important for dimerization and a nonconserved tail domain that is thought to interact with specific cargo (see Fig. 1). Kinesins bind MTs and a variety of cargoes and perform force-generating tasks such as transport of vesicles and organelles, spindle formation and elongation, chromosome segregation, and MT organization (Leopold et al., 1992; Sawin et al., 1992; Barton and Goldstein, 1996; Moore and Endow, 1996; Wein et al., 1996; Raich et al., 1998; Goldstein and Philip, 1999; Manning and Snyder, 1999; Reddy, 2001). Analysis of completed genome sequences of eukaryotes has resulted in identification of a large number of kinesins (Reddy and Day, 2001; Vale, 2003). Recently, all known kinesins have been grouped into 14 families that were designated as Kinesin-1 to Kinesin-14 (Lawrence et al., 2004). One of these families (Kinesin-14) possesses a C-terminal motor domain with minus-end motility, and the rest of the subfamilies have either an N-terminal or an internal motor domain (Fig. 1) and move toward the plus-end of MTs (Reddy and Day, 2001; Vale, 2003; Lawrence et al., 2004).
Plant kinesins were first identified in tobacco (Nicotiana tabacum) pollen tubes (pollen kinesin homolog) and tobacco phragmoplasts (tobacco kinesin related protein 125; Asada et al., 1991 ; Tiezzi et al., 1992; Cai et al., 1993). Since then, many kinesins have been identified in plants (Mitsui et al., 1993, 1994; Liu et al., 1996; Reddy et al., 1996a; Asada et al., 1997; Tamura et al., 1999; Barroso et al., 2000; Nishihama et al., 2002; Reddy, 2003; Tanaka et al., 2004). In Arabidopsis (Arabidopsis thaliana) alone there are at least 61 kinesins (Reddy and Day, 2001). Using genetic and cell biological approaches, functions of some plant kinesins have been reported (Reddy, 2003; Lee and Liu, 2004). Functional studies with a few kinesins have shown their involvement in mitosis and meiosis (Liu et al., 1996; Bowser and Reddy, 1997; Lee and Liu, 2000; Lee et al., 2001; Chen et al., 2002; Nishihama et al., 2002; Strompen et al., 2002; Yang et al., 2003; Pan et al., 2004; Ambrose et al., 2005), morphogenesis (Oppenheimer et al., 1997; Lu et al., 2005), and oriented deposition of cellulose myofibrils (Zhong et al., 2002). A kinesin that interacts with a geminivirus replication protein has also been reported in Arabidopsis (Kong and Hanley-Bowdoin, 2002). Predicted mitochondrial targeting sequences in two Arabidopsis kinesins mined from the database were shown to direct a green fluorescent protein fusion protein to mitochondria, suggesting that these kinesins are likely to function in these organelles (Itoh et al., 2001). A kinesin containing a calponin homology domain has been shown to interact with actin microfilaments, suggesting the involvement of some kinesins in coordinating actin and MT cytoskeleton (Preuss et al., 2004). The motility properties of only a few of these kinesins have been reported (Asada and Shibaoka, 1994; Song et al., 1997; Marcus et al., 2002).
A calmodulin-binding kinesin (kinesin-like calmodulin-binding protein [KCBP]) has been characterized from several flowering plants (Reddy et al., 1996a
Immunolocalization studies and antibody injection using antibodies specific to KCBP indicate that KCBP has a role in cell division (Bowser and Reddy, 1997
Searches of the National Center for Biotechnology Information (NCBI) and species-specific sequence databases have not identified a homolog of KCBP in the completely sequenced genomes of Saccharomyces cerevisiae, Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens, Cyanidioschyzon merolae, or Mus musculus (Miki et al., 2001 The presence of KCBP in flowering plants but not in fungal or animal genomes raises two questions. Is KCBP found in photosynthesizing organisms but not other eukaryote lineages, and what is the level of conservation of KCBP among phylogenetically divergent eukaryotes? To answer these questions, we have cloned and characterized KCBPs from a gymnosperm (Picea abies) and a green alga (Stichococcus bacillaris). In addition, we searched NCBI sequence databases and other databases of phylogenetically divergent photosynthetic and nonphotosynthetic eukaryotes for KCBP (See "Materials and Methods"). Gene tree analysis suggests that the KCBP-like motor domain originated prior to the divergence of plants and animals. However, the addition of the MyTH4 and talin-like domains appears to be limited to the plant lineage. Our data suggest that KCBP is highly conserved in land plants and green algae.
Cloning, Characterization, and Identification of KCBPs KCBP has been cloned from representative members of monocots and dicots and is highly conserved among angiosperms. In order to examine the presence and the level of conservation of unique domains in KCBP outside the angiosperms, we used PCR and library screening to clone KCBP from a gymnosperm (P. abies) and an alga (S. bacillaris). Primers corresponding to the conserved ATP-binding site of kinesins and the CBD of KCBP were used in PCR with P. abies cDNA library or S. bacillaris genomic DNA. PCR products from each species with sequences highly similar to KCBP from angiosperms were used as probes to screen the P. abies cDNA library and S. bacillaris library. Clones from the screens were isolated and sequenced. The predicted amino acid sequence (PaKCBP) of the longest isolated P. abies cDNA showed from 75% to 80.5% sequence identity to the motor domains of KCBPs from angiosperms. This clone contained the coding region for the motor domain and CBD. An S. bacillaris genomic clone was isolated that coded for a KCBP (SbKCBP, Fig. 2) with the unique KCBP domains (CBD, MyTH4, and talin-like region).
Using both the full-length and motor domain sequences of Arabidopsis KCBP (AtKCBP), we searched databases at NCBI, The Institute for Genomic Research (TIGR), and the Joint Genome Institute (JGI) including individual databases of species whose genomes are either completely sequenced or are being completed (see "Materials and Methods" for list of genomes searched), as well as expressed sequence tag (EST) databases, for the presence of KCBP homologs. KCBP sequences were identified only in land plants and green algae genomes (Table I). Using BLAST searches, full-length KCBPs were found in rice (Oryza sativa) and Chlamydomonas reinhardtii at NCBI and JGI, respectively. The rice amino acid sequence (OsKCBP) shows 90% similarity to Zea mays KCBP (ZmKCBP). The C. reinhardtii amino acid sequence (CrKCBP, Fig. 2) has the conserved-motor domain, CBD, coiled coil, MyTH4 region, and talin-like region found in other KCBPs. The sequence was originally generated from an unannotated scaffold (scaffold_633) DNA sequence using a splice site prediction program, two EST sequences, and comparison to the KCBP sequence. JGI has now annotated this sequence, and their annotation is in agreement with our generated sequence except that our sequence contains an additional sequence of about 100 amino acids at the N terminus, which is similar to other KCBPs. A scaffold sequence for a KCBP, which included the MyTH4, talin, coiled-coil, motor, and CBD domains, was also identified for Populus trichocarpa. Its sequence was closest to cotton KCBP. A KCBP-like sequence was found at http://moss.nibb.ac.jp/ for the moss Physcomitrella patens.
Fungi genomes including yeasts and plasmodium do not have a KCBP. It has been previously reported that KCBP is not present in the human, Drosophila, or C. elegans genomes (Miki et al., 2001 ; Reddy and Day, 2001; Siddiqui, 2002). Searches of other animal genomes (mouse, rat, dog, etc.) at http://www.ncbi.nih.gov/Genomes/index.html did not identify a KCBP in these species. Searches of the genomes at JGI resulted in identification of scaffold sequences with similarity to the KCBP motor domain (but did not contain the domains unique to KCBP) in the water molds Phytophthora sojae and Phytophthora ramoru and the diatom Thalassiora pseudonana. A scaffold sequence from Ciona intestinalis showed closest similarity to sea urchin SpKINC. The predicted Giardia lamblia amino acid sequence (G. lamblia kinesin-like protein [GlKLP]; Fig. 2) encodes a region of coiled coil followed by a kinesin motor domain that in BLAST searches showed the most similarity to KCBP motor domain from angiosperms. However, it does not contain the MyTH4, talin-like region, or CBD domain. A partial kinesin sequence in the protozoan Tetrahymena thermophila in TIGR also showed similarity to KCBP motor domain but lacked the CBD. Proteins were named KCBP if they were placed in the KCBP clade in our gene tree analysis (see below) and contained MyTH4, talin-like region, and CBD. Proteins that have motor domains most similar to KCBPs, but (1) lack MyTH4 and talin-like regions and (2) are not nested within the KCBP clade are not considered to be KCBPs.
A region that defines kinesin class specificity is the neck region, an approximately 45-amino acid-long segment that emerges from the catalytic core of the motor domain (Vale and Fletterick, 1997
A comparison of the sequence following the motor domain of known KCBPs and the KCBP-like proteins reported here is shown in Figure 3B. All reported KCBPs have a conserved CBD (70%–87% similar to AtKCBP) in this region. PaKCBP and CrKCBP show a high level of similarity to angiosperm CBDs (65% and 61%, respectively), while the SbKCBP sequence is more diverged (48%). A bacterially produced protein encompassing the CBD and motor domain of PaKCBP was shown to bind 35S calmodulin in the presence of Ca2+ but not in the presence of EGTA (data not shown). The sequence for the moss (P. patens) KCBP-like protein (PpKLP) shows 58% similarity to the CBD of AtKCBP. The sea urchin kinesin (SpKinC) showing similarity to the KCBP motor domain also contains a CBD, but the sequence is less conserved than the CBDs of angiosperm KCBPs (30% identical to AtKCBP). However, the bacterially expressed SpKinC has been shown to bind calmodulin (Rogers et al., 1999 ). A kinesin from C. intestinalis (CiKLP) also has a CBD that is 30% identical to AtKCBP and is similar to SpKinC (Fig. 3B). Although the binding of CiKLP to calmodulin has not been shown, it is likely that it also binds to calmodulin. The sequences following the motor domain in the T. thermophila and G. lamblia kinesin sequences have little similarity to the CBD of angiosperm KCBPs (9% and 13% identity to AtKCBP).
Supplemental data, consisting of the DIALIGN alignment, the data matrices, and the complete Bayesian and parsimony trees, are available online (Supplemental Figs. 1–5). The grouping of Arabidopsis kinesins in the complete trees is consistent with the earlier tree presented by Reddy and Day (2001)
Evolution of KCBP
Kull et al. (1998)
KCBP orthologs with the MyTH4, talin-like region, and CBD have been isolated from phylogenetically divergent land plants and green algae including Arabidopsis, tobacco, Solanum tuberosum, Z. mays, cotton (Reddy et al., 1996a
The only reported KCBP-like motor domain outside photosynthetic organisms is SpKinC isolated from sea urchin (Rogers et al., 1999
Our results show that complete KCBP with the N-terminal MyTH4 and talin-like regions, C-terminal motor, and CBD is found only in land plants and green algae. These results are consistent with the phylogeny of the eukaryotes, with the land plants and the green algae supported as a monophyletic group. (Baldauf, 2003
Functional studies with KCBP in flowering plants have shown its involvement in trichome morphogenesis and cell division (Bowser and Reddy, 1997
All reported KCBPs from land plants and green algae and SpKinC from sea urchin have a CBD at the C terminus that is responsible for regulating the interaction of the motor domain with MTs in a Ca2+-dependent manner (Song et al., 1997
The second proposition is that the common ancestor of KCBPs and SpKinC with a CBD existed before the divergence of plants and animals, which is believed to have occurred about 1.5 billion years ago (Wang et al., 1999
Materials Stichococcus bacillaris was grown in sterilized lake water enriched with Algo-Gro concentrate solution (Carolina Biological, Burlington, NC) at 18°C in a 16:8-h light/dark cycle. After 10 d, cells were collected by centrifugation and kept at –80°C for DNA isolation. Picea abies seeds, kindly provided by Dr. Peter Hedley (Scottish Crop Research Institute, Invergowire, UK) were germinated and grown on moist vermiculite in a growth chamber at 25°C for 3 weeks in white light (16 h light, 8 h dark). Seedlings were collected and stored at –80°C until use.
The KCBP motor domains of S. bacillaris and P. abies were amplified by PCR using either a cDNA library or genomic DNA as templates. Two degenerate primers, sense (5'-ATT/C/ATTT/CGCITAT/CGGICAA/GAC-3') and antisense (5'-CIGCT/CTGT/CTCT/CTTCCAG/ATA-3'), based on conserved motifs in the ATP and CBD in KCBP, were used to amplify approximately 2 kb and approximately 450 bp from S. bacillaris genomic DNA and P. abies cDNA, respectively. Sense and antisense primers contained restriction sites for EcoRI and BamHI, respectively. PCR reactions were performed in a final volume of 50 µL. The reaction mixtures were preheated at 94°C for 4 min and cooled to 50°C, and Taq polymerase was added to initiate the amplification reactions. Thirty-five cycles of amplification were performed in an Eppendorf Mastercycler Gradient (Eppendorf Scientific, Westbury, NY) followed by a final extension for 10 min. Each amplification cycle consisted of 1 min of denaturation at 94°C, 1 min of annealing at 50°C, and 2 min of extension at 72°C. After separation on an agarose gel, the PCR products were purified with Qiagen PCR purification kit (Qiagen USA, Valencia, CA), cloned into EcoRI/BamHI sites of Bluescript-KS+ vector (Stratagene, La Jolla, CA), verified by sequencing, and used as probes for library screening.
S. bacillaris genomic DNA was prepared from frozen cells using the urea-phenol-containing buffer method (Golovkin and Reddy, 1996
A P. abies cDNA library (kindly provided by Dr. Peter Engstrom) had been constructed from female strobilus RNA using a cDNA synthesis kit (Pharmacia Biotech, Piscataway, NJ) in
PCR-amplified products as well as cDNA and genomic clones were sequenced using double-stranded DNAs as templates. Primer walking was used to obtain the complete sequences. Sequence analysis was performed using Sequencer (Genescale, Ann Arbor, MI) and Mac Vector sequence analysis software (International Biotechnologies, New Haven, CT). Searches for sequence similarity using nucleotide- and predicted-amino acid sequences were performed using the BLAST network service provided by the National Library of Medicine (http://www.ncbi.nlm.nih.gov). Splice sites were predicted using the NetplantGene (http://genome.cbs.dtu.dk/services/NetPGene/). Alignments were performed using MegAlign (DNASTAR, Madison, WI). Protein secondary structure and domain analyses were performed using Simple Modular Architecture Research Tool (SMART v.3.1, http://smart.embl-heidelberg.de/) and InterProScan (http://www.ebi.ac.uk/InterProScan/).
Searches were done using AtKCBP full-length sequence at NCBI (www.ncbi.nlm.nih.gov/BLAST/) and the databases available at www.ncbi.nlm.nih.gov/Genomes/index.html (Aspergillus, bee, cat, chicken, chimp, cow, dictyostelium, dog, frog, fruit fly, human, malaria, microbes, mosquito, mouse, nematode, pig, plant genomes, rat, sea urchin, sheep, and zebrafish). The dictyostelium database search site included the following species (*completed genomes): Cryptosporidium hominis, Cryptosporidium parvum, Plasmodium berghei strain ANKA, Plasmodium chabaudi, *Plasmodium falciparum 3D7, Plasmodium yoelii yoelii, Theileria annulata, Toxoplasma gondii, Giardia lamblia ATCC 50803, Entamoeba histolytica, Entamoeba histolytica HM-1:IMSS, Aspergillus fumigatus, Aspergillus nidulans FGSC A4, Aspergillus terreus ATCC 20542, Coccidioides immitis RS, Coccidioides posadasii C735, Gibberella zeae PH-1, Magnaporthe grisea 70-15, Neurospora crassa, Candida albicans SC5314, *Candida glabrata CBS138, *Debaryomyces hansenii CBS767, *Eremothecium gossypii, *Kluyveromyces lactis NRRL Y-1140, Eremothecium gossypii, Kluyveromyces waltii NCYC 2644, Naumovia castellii NRRL Y-12630, Saccharomyces bayanus 623-6C, Saccharomyces bayanus MCYC 623, *Saccharomyces cerevisiae, Saccharomyces kluyveri NRRL Y-12651, Saccharomyces kudriavzevii IFO 1802, Saccharomyces mikatae IFO 1815, Saccharomyces paradoxus NRRL Y-17217, *Yarrowia lipolytica CLIB99, *Schizosaccharomyces pombe, Coprinopsis cinerea okayama7#130, Cryptococcus neoformans var grubii H99, Cryptococcus neoformans var neoformans B-3501A, Cryptococcus neoformans var neoformans JEC21, Cryptococcus neoformans var neoformans JEC21, Phanerochaete chrysosporium RP-78, Ustilago maydis 521, *Encephalitozoon cuniculi, Anopheles gambiae str. PEST, Apis mellifera, Bombyx mori, *Drosophila melanogaster, Drosophila pseudoobscura, Drosophila yakuba, *Sea squirt (Ciona intestinalis), Ciona savignyi, Gallus gallus, Takifugu rubripes, Tetraodon nigroviridis, Brugia malayi, Caenorhabditis briggsae, *Caenorhabditis elegans, *Leishmania major, Trypanosoma brucei, and Trypanosoma cruzi. Databases representing animal, protista, fungi, and plant species at TIGR Sequence Search (http://tigrblast.tigr.org/tgi/) were searched using the Arabidopsis (Arabidopsis thaliana) KCBP motor domain sequence. The sequences at TIGR are tentative consensus and singleton EST sequences. Searches at the JGI (http://genome.jgi-psf.org/) included the following organisms: C. reinhardtii, C. intestinalis, Fugu rubripes, Homo sapiens, P. chrysosporium, Phytophthora ramorum, Phytophthora sojae, Populus trichocarpa Thalassiosira pseudonana, and Xenopus tropicalis.
The sequences included in this analysis are those from Reddy and Day (2001)
Amino acids from individual sequences that DIALIGN did not align were replaced with gaps. All gap-only positions were then removed from the alignment using ClustalX. The resulting alignment of 780 positions was then exported into MacClade 4.03 (Maddison and Maddison, 2001
Gene tree analyses were performed using amino acid characters. Although amino acid characters have problems with a type of convergence (Simmons, 2000
Gene tree inference was performed using both parsimony and Bayesian (Rannala and Yang, 1996
Bayesian tree searches were performed using MrBayes 3.0b4 (Huelsenbeck and Ronquist, 2001
The rooting of the kinesin family used by Goodson et al. (1994) Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor.
Supplemental data, consisting of the DIALIGN alignments, the data matrices and the complete Bayesian and parsimony jackknife trees are available online. Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession numbers AY515262 (PaKCBP) and AY515314 (StKCBP).
We thank Dr. Peter Engstrom for providing the spruce cDNA library. The C. reinhardtii sequence data were produced by the U.S. Department of Energy Joint Genome Institute, http://www.jgi.doe.gov/ and are provided for use in this publication only. Received February 7, 2005; returned for revision March 25, 2005; accepted March 26, 2005.
1 This work was supported by a grant from the National Science Foundation (to A.S.N.R.). 
[w] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.060913. * Corresponding author; e-mail reddy{at}colostate.edu; fax 970–491–0649.
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ABSTRACT
RESULTS AND DISCUSSION
" symbols. See the supplemental figures for members of these clades included in this analysis. Kinesin-14 family, which contains C-terminal kinesins, is shown on the right side of the figure. Kinesin-13 family members contain an internal-motor domain. The members of the other families have an N-terminal motor domain. At, Arabidopsis; An, Aspergillus nidulans; Ce, C. elegans; Cg, Cricetulus griseus; Ci; C. intestinalis, Cp, Cyanophora paradoxa; Cr, C. reinhardtii; Dm, D. melanogaster; Gh, cotton; Gl, G. lamblia; Hs, H. sapiens; Mm, M. musculus; Mt, M. truncatula; Nt, tobacco; Os, rice; Pa, P. abies; Pr, P. ramorum; Ps, P. sojae; Pt, P. trichocarpa; St, S. tuberosum; Sc, S. cerevisiae; Sb, S. bacillaris; Sp, sea urchin; Spo, Schizosaccharomyces pombe; Tp, T. pseudonana; Tt, T. thermophila; Xl, Xenopus laevis.
gt10 cloning vector. For screening, approximately 5 x 105 recombinant plaques from the P. abies cDNA library and the S. bacillaris genomic libraries were transferred to Hybond N+ (Amersham, Piscataway, NJ) membranes according to the manufacturer's procedures. Membranes were hybridized to a 32P-labeled, PCR-amplified product at 60°C in a solution containing 0.5 M sodium phosphate, pH 7.2, and 0.7% w/v SDS. These membranes were washed twice in 2x SSC, 0.1% SDS for 10 min at room temperature, then twice with 1x SSC, 0.1% SDS for 15 min at 60°C. After three rounds of screening, phage DNA from each clone was prepared using Qiagen Lambda purification kit and sequenced. 
