Abstract
Kinesins and dyneins are two superfamilies of microtubule motor proteins that regulate many diverse fundamental cellular and developmental processes including cell shape, cell division and intracellular transport as well as spatial and temporal organization of molecules and organelles within the eukaryotic cells. These motor proteins use chemical energy from ATP to move unidirectionally using microtubules as roadways or to regulate microtubule dynamics. This review focuses on a comparative analysis of kinesins in eukaryotes, especially in the green lineage and their roles in plants. Comprehensive comparative analysis of kinesins among completed genome sequences of animal and several photosynthetic eukaryotes ranging from algae to monocots revealed considerable expansion of kinesins in flowering plants. Much of this expansion is due to an increase in members of two families (Kinesin-7 and Kinesin-14). Of the fourteen recognized families of kinesins in eukaryotes, members of four families are not found in flowering plants. However, a group of plant-specific kinesins does not fall into any of the recognized families, and some plant kinesins form plant-specific clades inside of their respective families. Some known domains are found exclusively either in plant and animal lineages, suggesting their functional specialization. Arabidopsis has the highest number of kinesins of any known multicellular eukaryotes, including humans, with a total of 61 kinesins. Although the processes regulated by many plant kinesins are yet to be discovered, functions of some kinesins have been elucidated in recent years using cell biological, molecular and genetic approaches and these are discussed briefly here. In addition, insights into regulatory mechanisms of a unique plant Ca2+/CaM-interacting motor called kinesin-like calmodulin-binding protein (KCBP) obtained through biochemical assays and crystal structure studies of its motor domain alone and as a complex with a calcium-binding protein are presented.
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References
Abdel-Ghany SE, Day IS, Simmons MP, Kugrens P, Reddy AS (2005) Origin and evolution of Kinesin-like calmodulin-binding protein. Plant Physiol 138:1711–1722
Abdel-Ghany SE, Reddy ASN (2000) A novel calcium/calmodulin-regulated kinesin-like protein is highly conserved between monocots and dicots. DNA Cell Biol 19:567–578
Ambrose JC, Cyr R (2007) The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19:226–236
Asada T, Kuriyama R, Shibaoka H (1997) TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci 110:179–189
Bannigan A, Scheible WR, Lukowitz W, Fagerstrom C, Wadsworth P, Somerville C, Baskin TI (2007) A conserved role for kinesin-5 in plant mitosis. J Cell Sci 120:2819–2827
Banuelos S, Saraste M, Carugo KD (1998) Structural comparisons of calponin homology domains: implications for actin binding. Structure 6:1419–1431
Bowser J, Reddy ASN (1997) Localization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J 12:1429–1438
Chen C, Marcus A, Li W, Hu Y, Calzada JP, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409
Day IS, Miller C, Golovkin M, Reddy ASN (2000) Interaction of a kinesin-like calmodulin-binding protein with a protein kinase. J Biol Chem 275:13737–13745
Deavours BE, Reddy ASN, Walker RA (1998) Ca2+/calmodulin regulation of the Arabidopsis kinesin-like calmodulin- binding protein. Cell Motil Cytoskeleton 40:408–416
DeVeylder L, Segers G, Glab N, Van Montagu M, Inze D (1997) Identification of proteins interacting with the Arabidopsis Cdc2aAt protein. J Exp Bot 48:2114–2114
Folkers U, Berger J, Hulskamp M (1997) Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124:3779–3786
Frey N, Klotz J, Nick P (2009) Dynamic bridges–a calponin-domain kinesin from rice links actin filaments and microtubules in both cycling and non-cycling cells. Plant Cell Physiol 50:1493–1506
Hirokawa N, Noda Y (2008) Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol Rev 88:1089–1118
Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682–696
Hiwatashi Y, Obara M, Sato Y, Fujita T, Murata T, Hasebe M (2008) Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell 20:3094–3106
Hulskamp M (2000) How plants split hairs. Curr Biol 10:R308–R310
Itoh R, Fujiwara M, Yoshida S (2001) Kinesin-related proteins with a mitochondrial targeting signal. Plant Physiol 127:724–726
Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45:83–100
Kao Y-L, Deavours BE, Phelps KK, Walker R, Reddy ASN (2000) Bundling of microtubules by motor and tail domains of a kinesin-like calmodulin-binding protein from Arabidopsis: regulation by Ca2+/calmodulin. Biochem Biophys Res Commun 267:201–207
King SM (2000) The dynein microtubule motor. Biochem Biophys Acta 1496:60–75
Kong L-J, Hanley-Bowdoin L (2002) A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infecion. Plant Cell 14:1817–1832
Krishnakumar S, Oppenheimer DG (1999) Extragenic suppressors of the Arabidopsis zwi-3 mutation identify new genes that function in trichome branch formation and pollen tube growth. Development 126:3079–3088
Kull FJ, Sablin EP, Lau R, Fletterick RJ, Vale RD (1996) Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380:550–555
Lai C, Xiong J, Li X, Qin X (2009) A 43-bp A/T-rich element upstream of the kinesin gene AtKP1 promoter functions as a silencer in Arabidopsis. Plant Cell Rep 28:851–860
Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LSB, Goodson HV, Hirokawa N, Howard J, Malmerg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy ASN, Saxton WM, Schliwa M, Scholey JM, Vale RD, Walczak CE, Wordeman L (2004) A standardized kinesin nomenclature. J Cell Biol 167:19–22
Lawrence CJ, Morrie NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2:362–363
Lee YR, Li Y, Liu B (2007) Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19:2595–2605
Lee Y-RJ, Liu B (2000) Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr Biol 10:797–800
Lee YR, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136:3877–3883
Leinweber BD, Leavis PC, Grabarek Z, Wang CL, Morgan KG (1999) Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. Biochem J 344:117–123
Li XY, Wang HQ, Xu T, Cao QH, Ren DT, Liu GQ (2007) Molecular cloning, expression and biochemical property analysis of AtKP1, a kinesin gene from Arabidopsis thaliana. Chin Sci Bull 52:1339–1346
Lu L, Lee YR, Pan R, Maloof JN, Liu B (2005) An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell 16:811–823
Luo D, Oppenheimer DG (1999) Genetic control of trichome branch number in Arabidopsis: the roles of FURCA loci. Development 126:5547–5557
Marcus AI, Ambrose JC, Blickley L, Hancock WO, Cyr RJ (2002) Arabidopsis thaliana protein, ATK1, is a minus-end directed kinesin that exhibits non-processive movement. Cell Motil Cytoskeleton 52:144–150
Marcus AI, Li W, Ma H, Cyr RJ (2003) A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14:1717–1726
Miki H, Okada Y, Hirokawa N (2005) Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15:467–476
Muller S, Han S, Smith LG (2006) Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16:888–894
Narasimhulu SB, Kao Y-L, Reddy ASN (1997) Interaction of Arabidopsis kinesin-like calmodulin-binding protein with tubulin subunits: modulation by Ca2+-calmodulin. Plant J 12:1139–1149
Narasimhulu SB, Reddy ASN (1998) Characterization of microtubule binding domains in the Arabidopsis kinesin-like calmodulin-binding protein. Plant Cell 10:957–965
Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H, Asada T, Irie K, Ito M, Terada M, Banno H, Yamazaki Y, Machida Y (2002) Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109:87–99
Oh SA, Bourdon V, Das ‘Pal M, Dickinson H, Twell D (2008) Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol Plant 1:794–799
Oppenheimer DG, Pollock MA, Vacik J, Szymanski DB, Ericson B, Feldmann K, Marks D (1997) Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc Natl Acad Sci USA 94:6261–6266
Pan R, Lee YR, Liu B (2004) Localization of two homologous Arabidopsis kinesin-related proteins in the phragmoplast. Planta 220:156–164
Preuss ML, Kovar DR, Lee YR, Staiger CJ, Delmer DP, Liu B (2004) A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136:3945–3955
Quan L, Xiao R, Li W, Oh SA, Kong H, Ambrose JC, Malcos JL, Cyr R, Twell D, Ma H (2008) Functional divergence of the duplicated AtKIN14a and AtKIN14b genes: critical roles in Arabidopsis meiosis and gametophyte development. Plant J 53:1013–1026
Reddy ASN, Day IS (2000) The role of the cytoskeleton and a molecular motor in trichome morphogenesis. Trends Plant Sci 5:503–505
Reddy AS, Day IS (2001) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2:Research0024.0021–0024.0017
Reddy ASN, Day IS (2001) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2
Reddy VS, Day IS, Thomas T, Reddy AS (2004) KIC, a novel Ca2+ binding protein with one EF-hand motif, interacts with a microtubule motor protein and regulates trichome morphogenesis. Plant Cell 16:185–200
Reddy VS, Reddy AS (2002) The calmodulin-binding domain from a plant kinesin functions as a modular domain in conferring Ca2+-CaM regulation to animal plus- and minus-end kinesins. J Biol Chem 277(50):48058–48065
Reddy VS, Reddy AS (2004) Developmental and cell-specific expression of ZWICHEL is regulated by the intron and exon sequences of its gene. Plant Mol Biol 54:273–293
Reddy ASN, Safadi F, Narasimhulu SB, Golovkin M, Hu X (1996) A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain. J Biol Chem 271:7052–7060
Reddy V, Safadi F, Zielinski RE, Reddy ASN (1999) Interaction of a kinesin-like protein with calmodulin isoforms from Arabidopsis. J Biol Chem 274:31727–31733
Richardson DN, Simmons MP, Reddy AS (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7:18
Rogers GC, Hart CL, Wedman KP, Scholey JM (1999) Identification of kinesin-C, a calmodulin-binding carboxy-terminal kinesin in animal (Strongylocentrotus purpuratus) cells. J Mol Biol 294:1–8
Sablin EP, Kull FJ, Cooke R, Vale RD, Fletterick RJ (1996) Crystal structure of the motor domain of the kinesin-related motor ncd. Nature 380:555–559
Sakai T, van der Honing H, Nishioka M, Uehara Y, Takahashi M, Fujisawa N, Saji K, Seki M, Shinozaki K, Jones MA, Smirnoff N, Okada K, Wasteneys GO (2008) Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J 53:157–171
Sharp DJ (2000) Microtubule motors in mitosis. Nature 407:41–47
Smirnova E, Reddy ASN, Bowser J, Bajer AS (1997) Distribution of kinesin-like minus end-directed protein during mitosis in endosperm of higher plant Haemanthus. Mol Biol Cell 8:378a
Song H, Golovkin M, Reddy ASN, Endow SA (1997) In vitro motility of AtKCBP, a calmodulin-binding kinesin-like protein of Arabidopsis. Proc Natl Acad Sci USA 94:322–327
Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jurgens G, Mayer U (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol 12:153–158
Takahashi Y, Soyano T, Sasabe M, Machida Y (2004) A MAP kinase cascade that controls plant cytokinesis. J Biochem 136:127–132
Tamura K, Nakatani K, Mitsui H, Ohashi Y, Takahashi H (1999) Characterization of katD, a kinesin-like protein gene specifically expressed in floral tissues of Arabidopsis thaliana. Gene 230:23–32
Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T, Machida C, Machida Y (2004) The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells 9:1199–1211
Tokai N, Fujimoto-Nishiyama A, Toyoshima Y, Yonemure S, Tsukita S, Inoue J, Yamamoto T (1996) Kid, a novel kinesin-like DNA binding protein, is localized to chromosomes and the mitotic spindle. EMBO J 15:457–467
Vanstraelen M, Inze D, Geelen D (2006) Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci 11:167–175
Vanstraelen M, Torres Acosta JA, DeVeylder L, Inze D, Greelen D (2004) A plant-specific subclass of C-terminal kinesins contains a conserved a-type cyclin-dependent kinase site implicated in folding and dimerization. Plant Physiol 135:141–1429
Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10:765–777
Vinogradova MV, Malanina GG, Reddy AS, Fletterick RJ (2009) Structure of the complex of a mitotic kinesin with its calcium binding regulator. Proc Natl Acad Sci USA 106:8175–8179
Vinogradova MV, Malanina GG, Reddy VS, Reddy AS, Fletterick RJ (2008) Structural dynamics of the microtubule binding and regulatory elements in the kinesin-like calmodulin binding protein. J Struct Biol 163:76–83
Vinogradova MV, Reddy VS, Reddy AS, Sablin EP, Fletterick RJ (2004) Crystal structure of kinesin regulated by Ca(2+)-calmodulin. J Biol Chem 279:23504–23509
Voss JW, Safadi F, Reddy ASN, Hepler PK (2000) The kinesin-like calmodulin binding protein is differentially involved in cell division. Plant Cell 12:979–990
Walker KL, Muller S, Moss D, Ehrhardt DW, Smith LG (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17:1827–1836
Weber KL, Sokac AM, Berg JS, Cheney RE, Bement WM (2004) A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature 431:325–329
Wei L, Zhang W, Liu Z, Li Y (2009) AtKinesin-13A is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol 9:138
Wickstead B, Gull K (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8:1708–1721
Xiong JY, Lai CX, Qu Z, Yang XY, Qin XH, Liu GQ (2009) Recruitment of AtWHY1 and AtWHY3 by a distal element upstream of the kinesin gene AtKP1 to mediate transcriptional repression. Plant Mol Biol 71:437–449
Xu T, Qu Z, Yang X, Qin X, Xiong J, Wang Y, Ren D, Liu G (2009) A cotton kinesin GhKCH2 interacts with both microtubules and microfilaments. Biochem J 421:171–180
Xu T, Sun X, Jiang S, Ren D, Liu G (2007) Cotton GhKCH2, a plant-specific kinesin, is low-affinitive and nucleotide-independent as binding to microtubule. J Biochem Mol Biol 40:723–730
Yamazaki H, Nakata T, Okada Y, Hirokawa N (1996) Cloning and characterization of KAP3: a novel kinesin superfamily- associated protein of KIF3A/3B. Proc Natl Acad Sci USA 93:8443–8448
Yang G, Gao P, Zhang H, Huang S, Zheng ZL (2007) A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS One 2:e1074
Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG (2003) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34:229–240
Zhong R, Burk DH, Morrison WH 3rd, Ye ZH (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101–3117
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Reddy, A.S.N., Day, I.S. (2011). Microtubule Motor Proteins in the Eukaryotic Green Lineage: Functions and Regulation. In: Liu, B. (eds) The Plant Cytoskeleton. Advances in Plant Biology, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0987-9_6
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