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Microtubule Plus End-Tracking Proteins and Their Activities in Plants

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The Plant Cytoskeleton

Part of the book series: Advances in Plant Biology ((AIPB,volume 2))

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Abstract

Microtubules form a dynamic system of filaments that have essential roles in all eukaryotic cells. Although microtubules are well-conserved across eukaryotic phyla, the organization and function of the microtubule cytoskeleton has evolved in ways that set higher plants apart from other organisms. The mechanisms that underlie these differences are topics of long-standing interest to plant cell biologists. A feature that is a key to microtubule function is their dynamic nature; they usually exist in states of growth or shrinkage. Their ability to grow, depolymerize, and then re-grow in new directions allows them to explore the cytoplasm and to rearrange into different configurations as needed. Microtubules also function in concert with a fleet of proteins that regulate microtubule activities within the cell. This chapter focuses on a specialized group of microtubule associated proteins (MAPs) that localize to the more active or plus ends of microtubules. From their position at the active end of the microtubule, these plus end-tracking proteins, or +TIPs, have a large influence on microtubule behaviour. They regulate growth and shrinkage rates and mediate interactions of the microtubule end with other proteins or structures in the cell. A number of +TIPs have been identified from several organisms including plants. The proteins form a structurally and functionally diverse group that have very little in common aside from an affinity for microtubule plus ends. Current models propose that these proteins form a dynamic +TIP network that is remodelled to include different sets of proteins depending on the needs of the cell. Here we discuss the repertoire of +TIP families found in plants. Plant cells have homologs corresponding to several proteins with plus-end binding activity in other organisms. Analyses indicate that there is some functional conservation amongst these proteins, although there are also cases where the plant proteins have been modified to function in different ways. In addition to conserved proteins, plants use at least one +TIP family that is not found in other eukaryotic genomes and there are some families that appear to be absent in higher plant lineages. The research to date suggests that plants have a somewhat modified +TIP network which is uniquely suited to the needs of the plant cell.

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References

  1. Abe T, Hashimoto T (2005) Altered microtubule dynamics by expression of modified α-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43:191–204

    Article  CAS  PubMed  Google Scholar 

  2. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, De Zeeuw CI, Grosveld F, Galjart N (2001) CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104:923–935

    Article  CAS  PubMed  Google Scholar 

  3. Akhmanova A, Stehbens SJ, Yap AS (2009) Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 10:268–274

    Article  CAS  PubMed  Google Scholar 

  4. Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309–322

    Article  CAS  PubMed  Google Scholar 

  5. Ambrose JC, Cyr R (2007) The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19:226–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ambrose JC, Cyr R (2008) Mitotic spindle organization by the preprophase band. Mol Plant 1:950–960

    Article  CAS  PubMed  Google Scholar 

  7. Ambrose JC, Li W, Marcus A, Ma H, Cyr R (2005) A minus-end-directed kinesin with plus-end tracking protein activity is Iivolved in spindle morphogenesis. Mol Biol Cell 16:1584–1592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19:2763–2775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ambrose JC, Wasteneys GO (2008) CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Mol Biol Cell 19:4730–4737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Aoki K, Taketo MM (2007) Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci 120:3327–3335

    Article  CAS  PubMed  Google Scholar 

  11. Askham JM, Vaughan KT, Goodson HV, Morrison EE (2002) Evidence that an interaction between EB1 and p150Glued is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol Biol Cell 13:3627–3645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Bannigan A, Lizotte-Waniewski M, Riley M, Baskin TI (2008) Emerging molecular mechanisms that power and regulate the anastral mitotic spindle of flowering plants. Plant Cell Physiol 65:1–11

    CAS  Google Scholar 

  13. Bartolini F, Gundersen GG (2006) Generation of noncentrosomal microtubule arrays. J Cell Sci 119:4155–4163

    Article  CAS  PubMed  Google Scholar 

  14. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG (2008) The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 181:523–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Berrueta L, Kraeft S-K, Tirnauer JS, Schuyler SC, Chen LB, Hill DE, Pellman D, Bierer BE (1998) The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc Natl Acad Sci U S A 95:10596–10601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665

    Article  CAS  PubMed  Google Scholar 

  17. Bieling P, Laan L, Schek H, Munteanu EL, Sandblad L, Dogterom M, Brunner D, Surrey T (2007) Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450:1100–1105

    Article  CAS  PubMed  Google Scholar 

  18. Bill Wickstead KG (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8:1708–1721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Bisgrove SR, Hable WE, Kropf DL (2004) +TIPs and microtubule regulation. The beginning of the plus end in plants. Plant Physiol 136:3855–3863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bisgrove SR, Lee YR, Liu B, Peters NT, Kropf DL (2008) The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant Cell 20:396–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Brandner K, Sambade A, Boutant E, Didier P, Mely Y, Ritzenthaler C, Heinlein M (2008) Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol 147:611–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, Howard J, Hyman AA (2008) XMAP215 is a processive microtubule polymerase. Cell 132:79–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bu W, Su L-K (2003) Characterization of functional domains of human EB1 family proteins. J Biol Chem 278:49721–49731

    Article  CAS  PubMed  Google Scholar 

  24. Cai G (2010) Assembly and disassembly of plant microtubules: tubulin modifications and binding to MAPs. J Exp Bot 61:623–626

    Article  CAS  PubMed  Google Scholar 

  25. Chan J, Calder G, Fox S, Lloyd C (2005) Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17:1737–1748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5:967–971

    Article  CAS  PubMed  Google Scholar 

  27. Chretien D, Fuller SD, Karsenti E (1995) Structure of growing microtubule ends: two dimensional sheets close into tubes at variable rates. J Cell Biol 129:1311–1328

    Article  CAS  PubMed  Google Scholar 

  28. Chretien D, Janosi I, Taveau J-C, Flyvbjerg H (1999) Microtubule’s conformational cap. Cell Struct Funct 24:299–303

    Article  CAS  PubMed  Google Scholar 

  29. Collings DA, Lill AW, Himmelspach R, Wasteneys GO (2006) Hypersensitivity to cytoskeletal antagonists demonstrates microtubule-microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytol 170:275–290

    Article  CAS  PubMed  Google Scholar 

  30. Coquelle FM, Vitre B, Arnal I (2009) Structural basis of EB1 effects on microtubule dynamics. Biochem Soc Trans 37:997–1001

    Article  CAS  PubMed  Google Scholar 

  31. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof Y-D, 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 21:1141–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. des Georges A, Katsuki M, Drummond DR, Osei M, Cross RA, Amos LA (2008) Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice. Nat Struct Mol Biol 15:1102–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Ann Rev Cell Dev Biol 13:83–117

    Article  CAS  Google Scholar 

  34. Dhonukshe P, Gadella TWJJ (2003) Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15:596–611

    Google Scholar 

  35. Dhonukshe P, Mathur J, Hulskamp M, Gadella TJ (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3:11–25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Dimitrov A, Quesnoit M, Moutel S, Cantaloube I, Pous C, Perez F (2008) Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science 322:1353–1356

    Article  CAS  PubMed  Google Scholar 

  37. Dixit R, Barnett J, Lazarus JE, Tokito M, Goldman YE, Holzbaur ELF (2009) Microtubule plus-end tracking by CLIP-170 requires EB1. Proc Natl Acad Sci U S A 106:492–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17:1298–1305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Dixit R, Cyr R (2004) Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16:3274–3284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Emons AM, Keelaar T (eds) (2009) Intracellular organization: a prerequisite for root hair elongation and cell wall deposition. Plant cell monograph, vol 12. Springer, Berlin, pp 27–44

    Google Scholar 

  41. Folker ES, Baker BM, Goodson HV (2005) Interactions between CLIP-170, tubulin, and microtubules: implications for the mechanism of CLIP-170 plus-end tracking behavior. Mol Biol Cell 16:5373–5384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Aarabidopsis thaliana. Development 127:4443–4453

    Article  CAS  PubMed  Google Scholar 

  43. Gard DL, Becker BE, Josh Romney S (2004) MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int Rev Cytol 239:179–272

    Article  CAS  PubMed  Google Scholar 

  44. Gard DL, Kirschner MW (1987) A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105:2203–2215

    Article  CAS  PubMed  Google Scholar 

  45. Gardiner J, Marc J (2003) Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 222:61–74

    Article  CAS  PubMed  Google Scholar 

  46. Geraldo S, Khanzada UK, Parsons M, Chilton JK, Gordon-Weeks PR (2008) Targeting of the F-actin-binding protein drebrin by the microtubule plus-tip protein EB3 is required for neuritogenesis. Nat Cell Biol 10:1181–1189

    Article  CAS  PubMed  Google Scholar 

  47. Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12:63–71

    Article  CAS  PubMed  Google Scholar 

  48. Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18:177–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Guo L, Ho C-HK, Kong Z, Lee Y-RJ, Qian Q, Liu B (2009) Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome. Ann Bot 103:387–402

    Article  CAS  PubMed  Google Scholar 

  50. Hayashi I, Ikura M (2003) Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J Biol Chem 278:36430–36434

    Article  CAS  PubMed  Google Scholar 

  51. Hayashi I, Wilde A, Mal TK, Ikura M (2005) Structural basis for the activation of microtubule assembly by the EB1 and p150Glued complex. Mol Cell 19:449–460

    Article  CAS  PubMed  Google Scholar 

  52. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, Grigoriev I, van Rijssel FJA, Buey RM, Lawera A, Jelesarov I, Winkler FK, Wüthrich K, Akhmanova A, Steinmetz MO (2009) An EB1-binding motif acts as a microtubule tip localization signal. Cell 138:366–376

    Article  CAS  PubMed  Google Scholar 

  53. Honnappa S, John CM, Kostrewa D, Winkler FK, Steinmetz MO (2005) Structural insights into the EB1-APC interaction. EMBO J 24:261–269

    Article  CAS  PubMed  Google Scholar 

  54. Honnappa S, Okhrimenko O, Jaussi R, Jawhari H, Jelesarov I, Winkler FK, Steinmetz MO (2006) Key interaction modes of dynamic +TIP networks. Mol Cell 23:663–671

    Article  CAS  PubMed  Google Scholar 

  55. Howard J, Hyman AA (2009) Growth, fluctuation and switching at microtubule plus ends. Nat Rev Mol Cell Biol 10:569–574

    Article  CAS  PubMed  Google Scholar 

  56. Hunter AW, Caplow M, Coy DL, Hancock WO, Diez S, Wordeman L, Howard J (2003) The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol Cell 11:445–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ishida T, Kaneko Y, Iwano M, Hashimoto T (2007) Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:8544–8549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Jiang K, Wang J, Liu J, Ward T, Wordeman L, Davidson A, Wang F, Yao X (2009) TIP150 interacts with and targets MCAK at the microtubule plus ends. EMBO 10:857–865

    Article  CAS  Google Scholar 

  59. Kawamura E, Himmelspach R, Rashbrooke MC, Whittington AT, Gale KR, Collings DA, Wasteneys GO (2006) MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol 140:102–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kawamura E, Wasteneys GO (2008) MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J Cell Sci 121:4114–4123

    Article  CAS  PubMed  Google Scholar 

  61. Ketelaar T, de Ruijter NC, Emons AM (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. King JS, Veltman DM, Georgiou M, Baum B, Insall RH (2010) SCAR/WAVE is activated at mitosis and drives myosin-independent cytokinesis. J Cell Sci 123:2246–2255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Komaki S, Abe T, Coutuer S, Inze D, Russinova E, Hashimoto T (2010) Nuclear-localized subtype of end-binding 1 protein regulates spindle organization in Arabidopsis. J Cell Sci 123:451–459

    Article  CAS  PubMed  Google Scholar 

  64. Komarova Y, De Groot CO, Grigoriev I, Gouveia SM, Munteanu EL, Schober JM, Honnappa S, Buey RM, Hoogenraad CC, Dogterom M, Borisy GG, Steinmetz MO, Akhmanova A (2009) Mammalian end binding proteins control persistent microtubule growth. J Cell Biol 184:691–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Korinek WS, Copeland MJ, Chaudhuri A, Chant J (2000) Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science 287:2257–2259

    Article  CAS  PubMed  Google Scholar 

  66. Kronja I, Kruljac-Letunic A, Caudron-Herger M, Bieling P, Karsenti E (2009) XMAP215-EB1 interaction is required for proper spindle assembly and chromosome segregation in Xenopus egg extract. Mol Biol Cell 20:2684–2696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kumar P, Lyle KS, Gierke S, Matov A, Danuser G, Wittmann T (2009) GSK3b phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J Cell Biol 184:895–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lansbergen G, Akhmanova A (2006) Microtubule plus end: a hub of cellular activities. Traffic 7:499–507

    Article  CAS  PubMed  Google Scholar 

  69. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LSB, Goodson HV, Hirokawa N, Howard J, Malmberg 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Lawrence CJ, Morris NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2:362–363

    Article  CAS  PubMed  Google Scholar 

  71. Ledbetter MC, Porter KR (1963) A “microtubule” in plant cell fine structure. J Cell Biol 19:239–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Lee L, Tirnauer JS, Li J, Schuyler SC, Liu JY, Pellman D (2000) Positioning of the mitotic spindle by a cortical microtubule capture mechanism. Science 287:2260–2262

    Article  CAS  PubMed  Google Scholar 

  73. Lee T, Langford KJ, Askham JM, Bruning-Richardson A, Morrison EE (2008) MCAK associates with EB1. Oncogene 27:2494–2500

    Article  CAS  PubMed  Google Scholar 

  74. Lee W-L, Bezanilla M, Pollard TD (2000) Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol 151:789–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lee Y-RJ, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136:3877–3883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lee YJ, Yang Z (2008) Tip growth: signaling in the apical dome. Curr Opin Plant Biol 11:662–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ligon LA, Shelly SS, Tokito M, Holzbaur ELF (2003) The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol Biol Cell 14:1405–1417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Louie RK, Bahmanyar S, Siemers KA, Votin V, Chang P, Stearns T, Nelson WJ, Barth AIM (2004) Adenomatous polyposis coli and EB1 localize in close proximity of the mother centriole and EB1 is a functional component of centrosomes. J Cell Sci 117:1117–1128

    Article  CAS  PubMed  Google Scholar 

  79. Lu L, Lee Y-RJ, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Maiato H, Fairley EAL, Rieder CL, Swedlow JR, Sunkel CE, Earnshaw WC (2003) Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 113:891–904

    Article  CAS  PubMed  Google Scholar 

  81. Maney T, Hunter AW, Wagenbach M, Wordeman L (1998) Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. J Cell Biol 142:787–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Manna T, Honnappa S, Steinmetz MO, Wilson L (2008) Suppression of microtubule dynamic instability by the +TIP protein EB1 and its modulation by the CAP-Gly domain of p150Glued. Biochemistry 47:779–786

    Article  CAS  PubMed  Google Scholar 

  83. Mathur J, Mathur N, Kernebeck B, Srinivas BP, Hulskamp M (2003) A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr Biol 13:1991–1997

    Article  CAS  PubMed  Google Scholar 

  84. Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  85. Miller RK, Cheng S-C, Rose MD (2000) Bim1p/Yeb1p mediates the Kar9p-dependent cortical attachment of cytoplasmic microtubules. Mol Biol Cell 11:2949–2959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Mimori-Kiyosue Y, Grigoriev I, Lansbergen G, Sasaki H, Matsui C, Severin F, Galjart N, Grosveld F, Vorobjev I, Tsukita S, Akhmanova A (2005) CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J Cell Biol 168:141–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000) Adenomatous Polyposis Coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol 148:505–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000) The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr Biol 10:865–868

    Article  CAS  PubMed  Google Scholar 

  89. Minc N, Bratman SV, Basu R, Chang F (2009) Establishing new sites of polarization by microtubules. Curr Biol 19:83–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242

    Article  CAS  PubMed  Google Scholar 

  91. Moore AT, Rankin KE, von Dassow G, Peris L, Wagenbach M, Ovechkina Y, Andrieux A, Job D, Wordeman L (2005) MCAK associates with the tips of polymerizing microtubules. J Cell Biol 169:391–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Morrison EE, Wardleworth BN, Askham JM, Markham AF, Meredith DM (1998) EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 17:3471–3477

    Article  CAS  PubMed  Google Scholar 

  93. Müller S, Wright AJ, Smith LG (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19:180–188

    Article  PubMed  CAS  Google Scholar 

  94. Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16:1178–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Nakajima K, Kawamura T, Hashimoto T (2006) Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol 47:513–522

    Article  CAS  PubMed  Google Scholar 

  96. Nakamura M, Zhou XZ, Lu KP (2001) Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr Biol 11:1062–1067

    Article  CAS  PubMed  Google Scholar 

  97. Niethammer P, Kronja I, Kandels-Lewis S, Rybina S, Bastiaens P, Karsenti E (2007) Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics. PLoS Biol 5:190–202

    Article  CAS  Google Scholar 

  98. Pedersen LB, Geimer S, Sloboda RD, Rosenbaum JL (2003) The microtubule plus end-tracking protein EB1 is localized to the flagellar tip and basal bodies in Chlamydomonas reinhardtii. Curr Biol 13:1969–1974

    Article  CAS  PubMed  Google Scholar 

  99. Pedersen LB, Miller MS, Geimer S, Leitch JM, Rosenbaum JL, Cole DG (2005) Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEB1, and regulates IFT at the flagellar tip. Curr Biol 15:262–266

    Article  CAS  PubMed  Google Scholar 

  100. Petrásek J, Schwarzerová K (2009) Actin and microtubule cytoskeleton interactions. Curr Opin Plant Biol 12:728–734

    Article  PubMed  CAS  Google Scholar 

  101. Reddy AS, Day IS (2001) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Rehberg M, Graf R (2002) Dictyostelium EB1 is a genuine centrosomal component required for proper spindle formation. Mol Biol Cell 13:2301–2310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Richardson DE, Simmons MP, Reddy ASN (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7:18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Robert S, Bichet A, Grandjean O, Kierzkowski D, Satiat-Jeunemaitre B, Pelletier S, Hauser M-T, Hofte H, Vernhettes S (2005) An Arabidopsis endo-1, 4-β-D-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17:3378–3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158:873–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Rogers SL, Wiedemann U, Hacker U, Turck C, Vale RD (2004) Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol 14:1827–1833

    Article  CAS  PubMed  Google Scholar 

  107. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GHH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Sandblad L, Busch KE, Tittmann P, Gross H, Brunner D, Hoenger A (2006) The Schizosaccharomyces pombe EB1 homolog Mal3p binds and stabilizes the microtubule lattice seam. Cell 127:1415–1424

    Article  CAS  PubMed  Google Scholar 

  109. Schmit A-C, Nick P (2008) Microtubules and the evolution of mitosis. In: Nick P (ed) Plant cell monograph, vol 11. Springer, Berlin, pp 234–266

    Google Scholar 

  110. Schober JM, Cain JM, Komarova YA, Borisy GG (2009) Migration and actin protrusion in melanoma cells are regulated by EB1 protein. Cancer Lett 284:30–36

    Article  CAS  PubMed  Google Scholar 

  111. Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20:759–779

    Article  CAS  PubMed  Google Scholar 

  112. Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR (2004) The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16:1506–1520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300:1715–1718

    Article  CAS  PubMed  Google Scholar 

  114. Sieberer BJ, Timmers CJ (2009) Microtubules in plant root hairs and their role in cell polarity and tip growth. In: Emons AM, Ketelaar T (eds) Plant cell monograph, vol 12. Springer, Berlin, pp 233–248

    Google Scholar 

  115. Simon JR, Salmon ED (1990) The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy. J Cell Sci 96:571–582

    Article  CAS  PubMed  Google Scholar 

  116. Skube SB, Chaverri JM, Goodson HV (2009) Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo. Cell Motil Cytoskeleton 67:1–12

    Google Scholar 

  117. Slep KC (2009) The role of TOG domains in microtubule plus end dynamics. Biochem Soc Trans 37:1002–1006

    Article  CAS  PubMed  Google Scholar 

  118. Slep KC (2010) Structural and mechanistic insights into microtubule end-binding proteins. Curr Opin Cell Biol 22:88–95

    Article  CAS  PubMed  Google Scholar 

  119. Slep KC, Rogers SL, Elliot SL, Okhura H, Kolodziej PA, Vale RD (2005) Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J Cell Biol 168:587–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Steinmetz MO, Akhmanova A (2008) Capturing protein tails by CAP-Gly domains. Trends Biochem Sci 33:535–545

    Article  CAS  PubMed  Google Scholar 

  121. Straube A, Brill M, Oakley BR, Horio T, Steinberg G (2003) Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol Biol Cell 14:642–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Su L-K, Burrell M, Hill DE, Gyuris J, Brent R, Wiltshire R, Trent J, Vogelstein B, Kinzler KW (1995) APC binds to the novel protein EB1. Cancer Res 55:2972–2977

    CAS  PubMed  Google Scholar 

  123. Tanaka K, Mukae N, Dewar H, van Breugel M, James EK, Prescott AR, Antony C, Tanaka TU (2005) Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434:987–994

    Article  CAS  PubMed  Google Scholar 

  124. Tirnauer JS, Canman JC, Salmon ED, Mitchison T (2002) EB1 targets to kinetochores with attached polymerizing microtubules. Mol Biol Cell 13:4308–4316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Tirnauer JS, Grego S, Salmon ED, Mitchison T (2002) EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol Biol Cell 13:3614–3626

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Tirnauer JS, O’Toole E, Berrueta L, Bierer BE, Pellman D (1999) Yeast Bim1p promotes the G1-specific dynamics of microtubules. J Cell Biol 145:993–1007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Tsvetkov AS, Samsonov A, Akhmanova A, Galjart N, Popov SV (2007) Microtubule-binding proteins CLASP1 and CLASP2 interact with actin filaments. Cell Motil Cytoskeleton 64:519–530

    Article  CAS  PubMed  Google Scholar 

  128. Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4:711–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Van Damme D, Bouget F-Y, Van Poucke K, Inze D, Geelen D (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40:386–398

    Article  PubMed  CAS  Google Scholar 

  130. Van Damme D, Van Poucke K, Boutant E, Ritzenthaler C, Inze D, Geelen D (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136:3956–3967

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. van der Vaart B, Akhmanova A, Straube A (2009) Regulation of microtubule dynamic instability. Biochem Soc Trans 37:1007–1013

    Article  PubMed  CAS  Google Scholar 

  132. Vaughan KT (2004) Surfing, regulating and capturing: are all microtubule-tip-tracking proteins created equal? Trends Cell Biol 14:491–496

    Article  CAS  PubMed  Google Scholar 

  133. Vaughan KT (2005) TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J Cell Biol 171:197–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Vitre B, Coquelle FM, Heichette C, Garnier C, Chretien D, Arnal I (2008) EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat Cell Biol 10:415–421

    Article  CAS  PubMed  Google Scholar 

  135. Vos JW, Dogterom M, Emons AMC (2004) Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search and capture” mechanism for microtubule translocation. Cell Motil Cytoskeleton 57:246–258

    Article  PubMed  Google Scholar 

  136. Walczak CE (2003) The Kin I kinesins are microtubule end-stimulated ATPases. Mol Cell 11:286–288

    Article  CAS  PubMed  Google Scholar 

  137. Walczak CE, Mitchison T, Desai A (1996) XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84:37–47

    Article  CAS  PubMed  Google Scholar 

  138. Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J. Cell Sci 115:1345–1354

    Article  CAS  Google Scholar 

  139. Wasteneys GO, Ambrose JC (2009) Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol 19:62–71

    Article  CAS  PubMed  Google Scholar 

  140. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJS, Chen M, Wallar BJ, Alberts AS, Gundersen GG (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6:820–830

    Article  CAS  PubMed  Google Scholar 

  142. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613

    Article  CAS  PubMed  Google Scholar 

  143. Wightman R, Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54:794–805

    Article  CAS  PubMed  Google Scholar 

  144. Wittmann T, Waterman-Storer CM (2005) Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3β in migrating epithelial cells. J Cell Biol 169:929–939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Yasuhara H, Muraoka M, Shogaki H, Mori H, Sonobe S (2002) TMBP200, a microtubule bundling polypeptide isolated from telophase tobacco BY-2 cells is a MOR1 homologue. Plant Cell Physiol 43:595–603

    Article  CAS  PubMed  Google Scholar 

  146. Zanic M, Stear JH, Hyman AA, Howard J (2009) EB1 recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS One 4:e7585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We would like to acknowledge Shannon Squires for performing the bioinformatic searches for the SxIP domain in the Arabidopsis databases. This work was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (Application 331017) awarded to S.R.B.

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  1. Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, BC, Canada, V5A 1S6

    Sherryl R. Bisgrove

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  1. Robin E. Young
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Correspondence to Sherryl R. Bisgrove .

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  1. Sect. Plant Biology, University of California, Shields Avenue 1, Davis, 95616, California, USA

    Bo Liu

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Young, R.E., Bisgrove, S.R. (2011). Microtubule Plus End-Tracking Proteins and Their Activities in Plants. 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_5

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