Protoplasma

, Volume 249, Issue 4, pp 887–899

Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins

Review Article

Abstract

Plants possess a large number of microtubule-based kinesin motor proteins. While the kinesin-2, 3, 9, and 11 families are absent from land plants, the kinesin-7 and 14 families are greatly expanded. In addition, some kinesins are specifically present only in land plants. The distinctive inventory of plant kinesins suggests that kinesins have evolved to perform specialized functions in plants. Plants assemble unique microtubule arrays during their cell cycle, including the interphase cortical microtubule array, preprophase band, anastral spindle and phragmoplast. In this review, we explore the functions of plant kinesins from a microtubule array viewpoint, focusing mainly on Arabidopsis kinesins. We emphasize the conserved and novel functions of plant kinesins in the organization and function of the different microtubule arrays.

Keywords

Plant Cortical microtubule Preprophase band Spindle Phragmoplast 

References

  1. Ambrose JC, Cyr R (2007) The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19(1):226–236PubMedCrossRefGoogle Scholar
  2. Ambrose JC, Li W, Marcus A, Ma H, Cyr R (2005) A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol Biol Cell 16(4):1584–1592PubMedCrossRefGoogle Scholar
  3. 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(Pt 2):179–189PubMedGoogle Scholar
  4. 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(Pt 16):2819–2827PubMedCrossRefGoogle Scholar
  5. Barroso C, Chan J, Allan V, Doonan J, Hussey P, Lloyd C (2000) Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J 24(6):859–868PubMedCrossRefGoogle Scholar
  6. Beck M, Komis G, Ziemann A, Menzel D, Samaj J (2011) Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 189(4):1069–1083PubMedCrossRefGoogle Scholar
  7. Bieling P, Telley IA, Surrey T (2010) A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 142(3):420–432PubMedCrossRefGoogle Scholar
  8. Bowser J, Reddy AS (1997) Localization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J 12(6):1429–1437PubMedCrossRefGoogle Scholar
  9. Cai G, Cresti M (2010) Microtubule motors and pollen tube growth—still an open question. Protoplasma 247(3–4):131–143PubMedCrossRefGoogle Scholar
  10. 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(10):2401–2409PubMedGoogle Scholar
  11. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21(4):1141–1154PubMedCrossRefGoogle Scholar
  12. Cyr R, Ambrose JC (2008) Mitotic spindle organization by the preprophase band. Mol Plant 1(6):950–960PubMedCrossRefGoogle Scholar
  13. Deavours BE, Reddy AS, Walker RA (1998) Ca2+/calmodulin regulation of the Arabidopsis kinesin-like calmodulin-binding protein. Cell Motil Cytoskeleton 40(4):408–416PubMedCrossRefGoogle Scholar
  14. Demonchy R, Blisnick T, Deprez C, Toutirais G, Loussert C, Marande W, Grellier P, Bastin P, Kohl L (2009) Kinesin 9 family members perform separate functions in the trypanosome flagellum. J Cell Biol 187(5):615–622PubMedCrossRefGoogle Scholar
  15. Duroc Y, Bouchez D, Pastuglia M (2011) The preprophase band and division site determination in land plants. In: Liu B (ed) The plant cytoskeleton. Springer, New York, pp 145–185CrossRefGoogle Scholar
  16. Ems-McClung SC, Walczak CE (2010) Kinesin-13s in mitosis: key players in the spatial and temporal organization of spindle microtubules. Semin Cell Dev Biol 21(3):276–282PubMedCrossRefGoogle Scholar
  17. Endow SA (1999) Determinants of molecular motor directionality. Nat Cell Biol 1(6):E163–E167PubMedCrossRefGoogle Scholar
  18. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20(1):45–58PubMedCrossRefGoogle Scholar
  19. 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(8):1493–1506PubMedCrossRefGoogle Scholar
  20. Frey N, Klotz J, Nick P (2010) A kinesin with calponin-homology domain is involved in premitotic nuclear migration. J Exp Bot 61(12):3423–3437PubMedCrossRefGoogle Scholar
  21. Furuta K, Toyoshima YY (2008) Minus-end-directed motor Ncd exhibits processive movement that is enhanced by microtubule bundling in vitro. Curr Biol 18(2):152–157PubMedCrossRefGoogle Scholar
  22. Goto Y, Asada T (2007) Excessive expression of the plant kinesin TBK5 converts cortical and perinuclear microtubules into a radial array emanating from a single focus. Plant Cell Physiol 48(5):753–761Google Scholar
  23. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11(7):797–806PubMedCrossRefGoogle Scholar
  24. Hirokawa N, Pfister KK, Yorifuji H, Wagner MC, Brady ST, Bloom GS (1989) Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell 56(5):867–878PubMedCrossRefGoogle Scholar
  25. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10(10):682–696PubMedCrossRefGoogle Scholar
  26. Ho CM, Hotta T, Guo F, Roberson RW, Lee YR, Liu B (2011) Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell. doi:10.1105/tpc.110.078204
  27. Hu CK, Coughlin M, Field CM, Mitchison TJ (2011) KIF4 regulates midzone length during cytokinesis. Curr Biol 21(10):815–824PubMedCrossRefGoogle Scholar
  28. Itoh R, Fujiwara M, Yoshida S (2001) Kinesin-related proteins with a mitochondrial targeting signal. Plant Physiol 127(3):724–726PubMedCrossRefGoogle Scholar
  29. Kao YL, Deavours BE, Phelps KK, Walker RA, Reddy AS (2000) Bundling of microtubules by motor and tail domains of a kinesin-like calmodulin-binding protein from Arabidopsis: regulation by Ca(2+)/Calmodulin. Biochem Biophys Res Commun 267(1):201–207PubMedCrossRefGoogle Scholar
  30. Komis G, Illes P, Beck M, Samaj J (2011) Microtubules and mitogen-activated protein kinase signalling. Curr Opin Plant Biol (in press)Google Scholar
  31. Kong LJ, 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 infection. Plant Cell 14(8):1817–1832PubMedCrossRefGoogle Scholar
  32. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LS, Goodson HV, Hirokawa N, Howard J, Malmberg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy AS, Saxton WM, Schliwa M, Scholey JM, Vale RD, Walczak CE, Wordeman L (2004) A standardized kinesin nomenclature. J Cell Biol 167(1):19–22PubMedCrossRefGoogle Scholar
  33. Lee YR, Liu B (2000) Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr Biol 10(13):797–800PubMedCrossRefGoogle Scholar
  34. Lee YR, Giang HM, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13(11):2427–2439PubMedGoogle Scholar
  35. Lee YR, Li Y, Liu B (2007) Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19(8):2595–2605PubMedCrossRefGoogle Scholar
  36. Li J, Jiang J, Qian Q, Xu Y, Zhang C, Xiao J, Du C, Luo W, Zou G, Chen M, Huang Y, Feng Y, Cheng Z, Yuan M, Chong K (2011) Mutation of rice BC12/GDD1, which encodes a kinesin-like protein that binds to a GA biosynthesis gene promoter, leads to dwarfism with impaired cell elongation. Plant Cell 23(2):628–640PubMedCrossRefGoogle Scholar
  37. Liu B, Cyr RJ, Palevitz BA (1996) A kinesin-like protein, KatAp, in the cells of arabidopsis and other plants. Plant Cell 8(1):119–132PubMedGoogle Scholar
  38. Liu B, Hotta T, Ho C-H, Lee YR (2011) Microtubule organization in the phragmoplast. In: Liu B (ed) The plant cytoskeleton. Springer, New York, pp 207–225CrossRefGoogle Scholar
  39. Lloyd C (2011) Dynamic microtubules and the texture of plant cell walls. Int Rev Cell Mol Biol 287:287–329PubMedCrossRefGoogle Scholar
  40. 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(2):811–823PubMedCrossRefGoogle Scholar
  41. Malcos JL, Cyr RJ (2011) An ungrouped plant kinesin accumulates at the preprophase band in a cell cycle-dependent manner. Cytoskeleton (Hoboken) 68(4):247–258Google Scholar
  42. 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(3):144–150PubMedCrossRefGoogle Scholar
  43. Marcus AI, Li W, Ma H, Cyr RJ (2003) A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14(4):1717–1726PubMedCrossRefGoogle Scholar
  44. Mathur J, Chua NH (2000) Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12(4):465–477PubMedGoogle Scholar
  45. Matsui K, Collings D, Asada T (2001) Identification of a novel plant-specific kinesin-like protein that is highly expressed in interphase tobacco BY-2 cells. Protoplasma 215(1–4):105–115Google Scholar
  46. Mazumdar M, Misteli T (2005) Chromokinesins: multitalented players in mitosis. Trends Cell Biol 15(7):349–355PubMedCrossRefGoogle Scholar
  47. Miki H, Okada Y, Hirokawa N (2005) Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15(9):467–476PubMedCrossRefGoogle Scholar
  48. Mucha E, Hoefle C, Huckelhoven R, Berken A (2010) RIP3 and AtKinesin-13A—a novel interaction linking Rho proteins of plants to microtubules. Eur J Cell Biol 89(12):906–916PubMedCrossRefGoogle Scholar
  49. Muller S, Han S, Smith LG (2006) Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16(9):888–894PubMedCrossRefGoogle Scholar
  50. Ni CZ, Wang HQ, Xu T, Qu Z, Liu GQ (2005) AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res 15(9):725–733PubMedCrossRefGoogle Scholar
  51. 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(1):87–99PubMedCrossRefGoogle Scholar
  52. 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(5):794–799PubMedCrossRefGoogle Scholar
  53. Oppenheimer DG, Pollock MA, Vacik J, Szymanski DB, Ericson B, Feldmann K, Marks MD (1997) Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc Natl Acad Sci USA 94(12):6261–6266PubMedCrossRefGoogle Scholar
  54. Pan R, Lee YR, Liu B (2004) Localization of two homologous Arabidopsis kinesin-related proteins in the phragmoplast. Planta 220(1):156–164PubMedCrossRefGoogle Scholar
  55. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495PubMedCrossRefGoogle Scholar
  56. 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(6):1013–1026PubMedCrossRefGoogle Scholar
  57. Reddy AS, Day IS (2001) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2(1):2PubMedCrossRefGoogle Scholar
  58. 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(1):185–200PubMedCrossRefGoogle Scholar
  59. Richardson DN, Simmons MP, Reddy AS (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7:18PubMedCrossRefGoogle Scholar
  60. Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol 48(2):345–361PubMedCrossRefGoogle Scholar
  61. Sakai T, 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(1):157–171PubMedCrossRefGoogle Scholar
  62. Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y (2011) Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal Behav 6(5):743–747PubMedCrossRefGoogle Scholar
  63. Shaw SL, Lucas J (2011) Intrabundle microtubule dynamics in the Arabidopsis cortical array. Cytoskeleton (Hoboken) 68(1):56–67Google Scholar
  64. Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300(5626):1715–1718PubMedCrossRefGoogle Scholar
  65. Smirnova EA, Reddy AS, Bowser J, Bajer AS (1998) Minus end-directed kinesin-like motor protein, Kcbp, localizes to anaphase spindle poles in Haemanthus endosperm. Cell Motil Cytoskeleton 41(3):271–280PubMedCrossRefGoogle Scholar
  66. Sparkes I (2011) Recent advances in understanding plant myosin function: life in the fast lane. Mol Plant. doi:10.1093/mp/ssr063
  67. 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(2):153–158PubMedCrossRefGoogle Scholar
  68. Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(19):8860–8865PubMedCrossRefGoogle Scholar
  69. Szymanski DB, Lloyd AM, Marks MD (2000) Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends Plant Sci 5(5):214–219PubMedCrossRefGoogle Scholar
  70. Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y (2010) HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 51(10):1766–1776PubMedCrossRefGoogle Scholar
  71. 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(12):1199–1211PubMedCrossRefGoogle Scholar
  72. Uchiyama Y, Sakaguchi M, Terabayashi T, Inenaga T, Inoue S, Kobayashi C, Oshima N, Kiyonari H, Nakagata N, Sato Y, Sekiguchi K, Miki H, Araki E, Fujimura S, Tanaka SS, Nishinakamura R (2009) Kif26b, a kinesin family gene, regulates adhesion of the embryonic kidney mesenchyme. Proc Natl Acad Sci USA 107(20):9240–9245CrossRefGoogle Scholar
  73. Umezu N, Umeki N, Mitsui T, Kondo K, Maruta S (2011) Characterization of a novel rice kinesin O12 with a calponin homology domain. J Biochem 149(1):91–101PubMedCrossRefGoogle Scholar
  74. Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112(4):467–480PubMedCrossRefGoogle Scholar
  75. Vale RD, Milligan RA (2000) The way things move: looking under the hood of molecular motor proteins. Science 288(5463):88–95PubMedCrossRefGoogle Scholar
  76. Vanstraelen M, Torres Acosta JA, De Veylder L, Inze D, Geelen 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(3):1417–1429PubMedCrossRefGoogle Scholar
  77. Vanstraelen M, Inze D, Geelen D (2006a) Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci 11(4):167–175PubMedCrossRefGoogle Scholar
  78. Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006b) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16(3):308–314PubMedCrossRefGoogle Scholar
  79. Vos JW, Safadi F, Reddy AS, Hepler PK (2000) The kinesin-like calmodulin binding protein is differentially involved in cell division. Plant Cell 12(6):979–990PubMedGoogle Scholar
  80. Wadsworth P, Lee WL, Murata T, Baskin TI (2011) Variations on theme: spindle assembly in diverse cells. Protoplasma 248(3):439–446PubMedCrossRefGoogle Scholar
  81. Walczak CE, Heald R (2008) Mechanisms of mitotic spindle assembly and function. Int Rev Cytol 265:111–158PubMedCrossRefGoogle Scholar
  82. Walker KL, Muller S, Moss D, Ehrhardt DW, Smith LG (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17(21):1827–1836PubMedCrossRefGoogle Scholar
  83. Wasteneys GO, Ambrose JC (2009) Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol 19(2):62–71PubMedCrossRefGoogle Scholar
  84. 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 9:138PubMedCrossRefGoogle Scholar
  85. Wickstead B, Gull K (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8(12):1708–1721PubMedCrossRefGoogle Scholar
  86. Wordeman L (2005) Microtubule-depolymerizing kinesins. Curr Opin Cell Biol 17(1):82–88PubMedCrossRefGoogle Scholar
  87. Wright AJ, Smith LG (2007) Division plane orientation in plant cells. In: Verma DP, Hong Z (eds) Cell division control in plants. Springer, Berlin, pp 33–57Google Scholar
  88. 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(5):723–730PubMedCrossRefGoogle Scholar
  89. Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Muller S, Meier I (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci USA 105(47):18637–18642PubMedCrossRefGoogle Scholar
  90. 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(2):171–180PubMedCrossRefGoogle Scholar
  91. 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(2):229–240PubMedCrossRefGoogle Scholar
  92. 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(10):e1074PubMedCrossRefGoogle Scholar
  93. Yang XY, Chen ZW, Xu T, Qu Z, Pan XD, Qin XH, Ren DT, Liu GQ (2011) Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. Plant Cell 23(3):1093–1106PubMedCrossRefGoogle Scholar
  94. Zhang M, Zhang B, Qian Q, Yu Y, Li R, Zhang J, Liu X, Zeng D, Li J, Zhou Y (2010) Brittle Culm 12, a dual-targeting kinesin-4 protein, controls cell-cycle progression and wall properties in rice. Plant J 63(2):312–328PubMedCrossRefGoogle Scholar
  95. 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(12):3101–3117PubMedCrossRefGoogle Scholar
  96. Zhou R, Niwa S, Homma N, Takei Y, Hirokawa N (2009) KIF26A is an unconventional kinesin and regulates GDNF-Ret signaling in enteric neuronal development. Cell 139(4):802–813PubMedCrossRefGoogle Scholar
  97. Zhu C, Dixit R (2011) Single molecule analysis of the Arabidopsis FRA1 kinesin shows that it is a functional motor protein with unusually high processivity. Mol Plant 4(5):879–885PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Biology DepartmentWashington UniversitySt. LouisUSA

Personalised recommendations