Microtubules, MAPs and Xylem Formation

  • Edouard Pesquet
  • Clive Lloyd
Part of the Advances in Plant Biology book series (AIPB, volume 2)


Xylem is essential for transporting water and minerals transport as well as for mechanical resistance against gravity. These key characteristics of xylem are enabled by the development of specific secondary cell walls which exhibit different patterns of thickening. Microtubules are associated with the sites at which the secondary thickenings develop and pharmacological and genetic modulation demonstrate that these cortical microtubules control the orientation, the patterning, the symmetry and the smoothness of the secondary wall.


Secondary Wall Secondary Cell Wall Cellulose Microfibril Cortical Microtubule Xylem Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Abe H, Funada R, Imaizumi H, Ohtani J, Fukazawa K (1995) Dynamic changes in the arrangement of cortical microtubules in conifer tracheids during differentiation. Planta 197:418–421CrossRefGoogle Scholar
  2. 2.
    Abe H, Funada R, Ohtani J, Fukazawa K (1995) Changes in the arrangement of microtubules and microfibrils in differentiating conifer tracheids during the expansion of cells. Ann Bot 75:305–310CrossRefGoogle Scholar
  3. 3.
    Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165PubMedCrossRefGoogle Scholar
  4. 4.
    Anthony RG, Hussey PJ (1998) Suppression of endogenous alpha and beta tubulin synthesis in transgenic maize calli overexpressing alpha and beta tubulins. Plant J 16:297–304PubMedCrossRefGoogle Scholar
  5. 5.
    Arend M, Fromm J (2003) Ultrastructural changes in cambial cell derivatives during xylem differentiation in poplar. Plant Biol 5:255–264CrossRefGoogle Scholar
  6. 6.
    Blume Y, Yemets A, Sulimenko V, Sulimenko T, Chan J, Lloyd C, Dräber P (2008) Tyrosine phosphorylation of plant tubulin. Planta 229:143–150PubMedCrossRefGoogle Scholar
  7. 7.
    Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546PubMedCrossRefGoogle Scholar
  8. 8.
    Brower DL, Hepler PK (1976) Microtubules and secondary wall deposition in xylem: the effects of isopropyl N-phenylcarbamate. Protoplasma 87:91–111PubMedCrossRefGoogle Scholar
  9. 9.
    Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827PubMedCrossRefGoogle Scholar
  10. 10.
    Burk DH, Ye ZH (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14:2145–2160PubMedCrossRefGoogle Scholar
  11. 11.
    Burk DH, Zhong R, Morrison WH, Ye ZH (2006) Disruption of cortical microtubules by overexpression of green fluorescent protein-tagged a-tubulin 6 causes a marked reduction in cell wall synthesis. J Integr Plant Biol 48:85–98CrossRefGoogle Scholar
  12. 12.
    Buschmann H, Lloyd CW (2008) Arabidopsis mutants and the network of microtubule-associated functions. Mol Plant 1:888–898PubMedCrossRefGoogle Scholar
  13. 13.
    Cai G (2010) Assembly and disassembly of plant microtubules: tubulin modifications and binding to MAPs. J Exp Bot 61:623–626PubMedCrossRefGoogle Scholar
  14. 14.
    Cai G, Ovidi E, Romagnoli S, Vantard M, Cresti M, Tiezzi A (2005) Identification and characterization of plasma membrane proteins that bind to microtubules in pollen tubes and generative cells of tobacco. Plant Cell Physiol 46:563–578PubMedCrossRefGoogle Scholar
  15. 15.
    Celedon PAF, Andrade A, Meireles KGX et al (2007) Proteomic analysis of the cambial region in juvenile Eucalyptus grandis at three ages. Proteomics 7:2258–2274CrossRefGoogle Scholar
  16. 16.
    Chaffey NJ, Barnett JR, Barlow PW (1997) Cortical microtubule involvement in bordered pit formation in secondary xylem vessel elements of Aesculus hippocastanum L. (Hippocastanaceae): a correlative study using electron microscopy and indirect immunofluorescence microscopy. Protoplasma 197:64–75CrossRefGoogle Scholar
  17. 17.
    Chaffey NJ, Barnett JR, Barlow PW (1999) A cytoskeletal basis for wood formation in angiosperm trees: the involvement of cortical microtubules. Planta 208:19–30CrossRefGoogle Scholar
  18. 18.
    Chaffey N, Barlow P, Sundberg B (2002) Understanding the role of the cytoskeleton in wood formation in angiosperm trees: hybrid aspen (Populus tremula x P. tremuloides) as the model species. Tree Physiol 22:239–249PubMedGoogle Scholar
  19. 19.
    Chan J, Calder G, Fox S, Lloyd C (2007) Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 9:171–175PubMedCrossRefGoogle Scholar
  20. 20.
    Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW (1999) The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci U S A 96:14931–14936PubMedCrossRefGoogle Scholar
  21. 21.
    Chan J, Sambade A, Calder G, Lloyd C (2009) Arabidopsis cortical microtubules are initiated along, as well as branching from, existing microtubules. Plant Cell 21:2298–2306PubMedCrossRefGoogle Scholar
  22. 22.
    Cheng Z, Snustad DP, Carter JV (2001) Temporal and spatial expression patterns of TUB9, a beta-tubulin gene of Arabidopsis thaliana. Plant Mol Biol 47:389–398PubMedCrossRefGoogle Scholar
  23. 23.
    Chu B, Wilson TJ, McCune-Zierath C, Snustad DP, Carter JV (1998) Two beta-tubulin genes, TUB1 and TUB8, of Arabidopsis exhibit largely nonoverlapping patterns of expression. Plant Mol Biol 37:785–790PubMedCrossRefGoogle Scholar
  24. 24.
    Clayton L, Lloyd CW (1984) The relationship between the division plane and spindle geometry in Allium cells treated with CIPC and griseofulvin: an anti-tubulin study. Eur J Cell Biol 34:248–253PubMedGoogle Scholar
  25. 25.
    Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Höfte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21:1141–1154PubMedCrossRefGoogle Scholar
  26. 26.
    Déjardin A, Leplé JC, Lesage-Descauses MC, Costa G, Pilate G (2004) Expressed sequence tags from poplar wood tissues – a comparative analysis from multiple libraries. Plant Biol 6:55–64PubMedCrossRefGoogle Scholar
  27. 27.
    Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M, Matsuoka N, Minami A, Nagata-Hiwatashi M, Nakamura K, Okamura Y, Sassa N, Suzuki S, Yazaki J, Kikuchi S, Fukuda H (2002) Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc Natl Acad Sci U S A 99:15794–15799PubMedCrossRefGoogle Scholar
  28. 28.
    Duckett CM, Lloyd CW (1994) Gibberellic acid-induced microtubule reorientation in dwarf peas is accompanied by rapid modification of an a-tubulin isotype. Plant J 5:363–372CrossRefGoogle Scholar
  29. 29.
    Endo S, Pesquet E, Yamaguchi M, Tashiro G, Sato M, Toyooka K, Nishikubo N, Udagawa-Motose M, Kubo M, Fukuda H, Demura T (2009) Identifying new components participating in the secondary cell wall formation of vessel elements in zinnia and Arabidopsis. Plant Cell 21:1155–1165PubMedCrossRefGoogle Scholar
  30. 30.
    Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New YorkGoogle Scholar
  31. 31.
    Falconer MM, Seagull RW (1985) Immunofluorescent and calcofluor white staining of developing tracheary elements in Zinnia elegans L. suspension cultures. Protoplasma 125:190–198CrossRefGoogle Scholar
  32. 32.
    Falconer MM, Seagull RW (1985) Xylogenesis in tissue culture: taxol effects on microtubule reorientation and lateral association in differentiating cells. Protoplasma 128:157–166CrossRefGoogle Scholar
  33. 33.
    Falconer MM, Seagull RW (1986) Xylogenesis in tissue culture II: microtubules, cell shape and secondary wall patterns. Protoplasma 133:140–148CrossRefGoogle Scholar
  34. 34.
    Falconer MM, Seagull RW (1988) Xylogenesis in tissue culture III: continuing wall deposition during tracheary element differentiation. Protoplasma 144:10–16CrossRefGoogle Scholar
  35. 35.
    Fosket DE, Roberts LW (1964) Induction of wound-vessel differentiation in isolated coleus stem segments in vitro. Am J Bot 51:19–25CrossRefGoogle Scholar
  36. 36.
    Fukuda H (1987) A change in tubulin synthesis in the process of tracheary element differentiation and cell division of isolated zinnia mesophyll cells. Plant Cell Physiol 28:517–528Google Scholar
  37. 37.
    Fukuda H (1989) Regulation of tubulin degradation in isolated zinnia mesophyll cells in culture. Plant Cell Physiol 30:243–252Google Scholar
  38. 38.
    Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391PubMedCrossRefGoogle Scholar
  39. 39.
    Fukuda H, Kobayashi H (1989) Dynamic organization of the cytoskeleton during tracheary-element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Dev Growth Differ 31:9–16CrossRefGoogle Scholar
  40. 40.
    Funada R, Abe H, Furusawa O, Imaizumi H, Fukazawa K, Ohtani J (1997) The orientation and localization of cortical microtubules in differentiating conifer tracheids during cell expansion. Plant Cell Physiol 38:210–212Google Scholar
  41. 41.
    Funada R, Miura H, Shibagaki M, Furusawa O, Miura T, Fukatsu E, Kitin P (2001) Involvement of localized cortical microtubules in the formation of a modified structure of wood. J Plant Res 144:491–497CrossRefGoogle Scholar
  42. 42.
    Furusawa O, Funada R, Murakami Y, Ohtani J (1997) Arrangement of cortical microtubules in compression wood tracheids of Taxus cuspidata visualized by confocal laser microscopy. J Wood Sci 44:230–233CrossRefGoogle Scholar
  43. 43.
    Gaillard J, Neumann E, Van Damme D, Stoppin-Mellet V, Ebel C, Barbier E, Geelen D, Vantard M (2008) Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol Biol Cell 19:4534–4544PubMedCrossRefGoogle Scholar
  44. 44.
    Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158PubMedCrossRefGoogle Scholar
  45. 45.
    Gardiner JC, Taylor NG, Turner SR (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell 15:1740–1748PubMedCrossRefGoogle Scholar
  46. 46.
    Gion JM, Lalanne C, Le Provost G, Ferry-Dumazet H, Paiva J, Chaumeil P, Frigerio JM, Brach J, Barré A, de Daruvar A, Claverol S, Bonneu M, Sommerer N, Negroni L, Plomion C (2005) The proteome of maritime pine wood forming tissue. Proteomics 5:3731–3751PubMedCrossRefGoogle Scholar
  47. 47.
    González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409PubMedCrossRefGoogle Scholar
  48. 48.
    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 11:797–806PubMedCrossRefGoogle Scholar
  49. 49.
    Hamada T (2007) Microtubule-associated proteins in higher plants. J Plant Res 120:79–98PubMedCrossRefGoogle Scholar
  50. 50.
    Hammersley DRH, McCully ME (1980) Differentiation of wound xylem in pea roots in the presence of colchicines. Plant Sci Lett 19:151–156CrossRefGoogle Scholar
  51. 51.
    Heath W (1985) Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164:12–21CrossRefGoogle Scholar
  52. 52.
    Hepler PK, Fosket DE (1971) The role of microtubules in vessel member differentiation in Coleus. Protoplasma 72:213–236CrossRefGoogle Scholar
  53. 53.
    Hepler PK, Newcomb EH (1964) Microtubules and fibrils in the cytoplasm of coleus cells undergoing secondary wall deposition. J Cell Biol 20:529–532PubMedCrossRefGoogle Scholar
  54. 54.
    Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhlén M, Teeri TT, Lundeberg J, Sundberg B, Nilsson P, Sandberg G (2001) A transcriptional roadmap to wood formation. Proc Natl Acad Sci U S A 98:14732–14737PubMedCrossRefGoogle Scholar
  55. 55.
    Hogetsu T (1991) Mechanism for formation of the secondary wall thickening in tracheary elements: Microtubules and microfibrils of tracheary elements of Pisum sativum L. and Commelina communis L. and the effects of amiprophosmethyl. Planta 185:190–200CrossRefGoogle Scholar
  56. 56.
    Huang RF, Lloyd CW (1999) Gibberellic acid stabilizes microtubules in maize suspension cells to cold and stimulates acetylation of a-tubulin. FEBS Lett 443:317–320PubMedCrossRefGoogle Scholar
  57. 57.
    Jovanovic AM, Durst S, Nick P (2010) Plant cell division is specifically affected by nitrotyrosine. J Exp Bot 61:901–909PubMedCrossRefGoogle Scholar
  58. 58.
    Juan D, Hong-Li X, De-Qiang Z, Xin-Qiang H, Min-Jie W, Ying-Zhang L, Ke-Ming C, Lu Meng-Zhu L (2006) Regeneration of the secondary vascular system in poplar as a novel system to investigate gene expression by a proteomic approach. Proteomics 6:881–895CrossRefGoogle Scholar
  59. 59.
    Kaneda M, Rensing K, Samuels L (2010) Secondary cell wall deposition in developing secondary xylem of poplar. J Integr Plant Biol 52:234–243PubMedCrossRefGoogle Scholar
  60. 60.
    Kobayashi H, Fukuda H, Shibaoka H (1988) Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in cultured Zinnia cells. Protoplasma 143:29–37CrossRefGoogle Scholar
  61. 61.
    Kopczak SD, Haas NA, Hussey PJ, Silflow CD, Snustad DP (1992) The small genome of Arabidopsis contains at least six expressed alpha-tubulin genes. Plant Cell 4:539–547PubMedCrossRefGoogle Scholar
  62. 62.
    Korolev AV, Buschmann H, Doonan JH, Lloyd CW (2007) AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci 120:2241–2247PubMedCrossRefGoogle Scholar
  63. 63.
    Korolev AV, Chan J, Naldrett MJ, Doonan JH, Lloyd CW (2005) Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells. Plant J 42:547–555PubMedCrossRefGoogle Scholar
  64. 64.
    Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860PubMedCrossRefGoogle Scholar
  65. 65.
    Le J, Vandenbussche F, De Cnodder T, Van der Straeten D, Verbelen J-P (2005) Cell elongation and microtubule behavior in Arabidopsis hypocotyl: responses to ethylene and auxin. J Plant Growth Reg 24:166–178CrossRefGoogle Scholar
  66. 66.
    Lee YR, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136:3877–3883PubMedCrossRefGoogle Scholar
  67. 67.
    Li X, Wu HX, Dillon SK, Southerton SG (2009) Generation and analysis of expressed sequence tags from six developing xylem libraries in Pinus radiata D. Don. BMC Genomics 10:41–59PubMedCrossRefGoogle Scholar
  68. 68.
    Li X, Wu HX, Southerton SG (2010) Seasonal reorganization of the xylem transcriptome at different tree ages reveals novel insights into wood formation in Pinus radiata. New Phytol 187:764–776PubMedCrossRefGoogle Scholar
  69. 69.
    Liang BM, Dennings AM, Sharp RE, Baskin TI (1996) Consistent handedness of microtubule helical arrays in maize and Arabidopsis primary roots. Protoplasma 190:8–15CrossRefGoogle Scholar
  70. 70.
    Mao G, Buschmann H, Doonan JH, Lloyd CW (2006) The role of MAP65-1 in microtubule bundling during Zinnia tracheary element formation. J Cell Sci 119:753–758PubMedCrossRefGoogle Scholar
  71. 71.
    Morejohn LC, Bureau TE, Tocchi LP, Fosket DE (1984) Tubulins from different higher plant species are immunologically nonidentical and bind colchicine differentially. Proc Natl Acad Sci U S A 81:1440–1444PubMedCrossRefGoogle Scholar
  72. 72.
    Murmanis L (1971) Particles and microtubules in vascular cells of Pinus strobes L. during cell wall formation. New Phytol 70:1089–1093CrossRefGoogle Scholar
  73. 73.
    Nagawa S, Sawa S, Sato S, Kato T, Tabata S, Fukuda H (2006) Gene trapping in Arabidopsis reveals genes involved in vascular development. Plant Cell Physiol 47:1394–1405PubMedCrossRefGoogle Scholar
  74. 74.
    Nelmes BJ, Preston RD, Ashworth D (1973) A possible function of microtubules suggested by their abnormal distribution in rubbery wood. J Cell Sci 13:741–751PubMedGoogle Scholar
  75. 75.
    Oda Y, Mimura T, Hasezawa S (2005) Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–1036PubMedCrossRefGoogle Scholar
  76. 76.
    Oda Y, Lida Y, Kondo Y, Fukuda H (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 20:1197–1202PubMedCrossRefGoogle Scholar
  77. 77.
    Oakley RV, Wang YS, Ramakrishna W, Harding SA, Tsai CJ (2007) Differential expansion and expression of alpha- and beta-tubulin gene families in Populus. Plant Physiol 145:961–973PubMedCrossRefGoogle Scholar
  78. 78.
    Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495PubMedCrossRefGoogle Scholar
  79. 79.
    Paiva JA, Garcés M, Alves A, Garnier-Géré P, Rodrigues JC, Lalanne C, Porcon S, Le Provost G, Perez Dda S, Brach J, Frigerio JM, Claverol S, Barré A, Fevereiro P, Plomion C (2008) Molecular and phenotypic profiling from the base to the crown in maritime pine wood-forming tissue. New Phytol 178:283–301PubMedCrossRefGoogle Scholar
  80. 80.
    Paiva JA, Garnier-Géré PH, Rodrigues JC, Alves A, Santos S, Graça J, Le Provost G, Chaumeil G, Da Silva-Perez D, Bosc A, Fevereiro P, Plomion C (2008) Plasticity of maritime pine (Pinus pinaster) wood-forming tissues during a growing season. New Phytol 179:1080–1094PubMedCrossRefGoogle Scholar
  81. 81.
    Paux E, Carocha V, Marques C, Mendes de Sousa A, Borralho N, Sivadon P, Grima-Pettenati J (2005) Transcript profiling of Eucalyptus xylem genes during tension wood formation. New Phytol 167:89–100PubMedCrossRefGoogle Scholar
  82. 82.
    Paux E, Tamasloukht M, Ladouce N, Sivadon P, Grima-Pettenati J (2004) Identification of genes preferentially expressed during wood formation in Eucalyptus. Plant Mol Biol 55:263–280PubMedCrossRefGoogle Scholar
  83. 83.
    Pickett-Heaps JD (1967) The effects of colchicine on the ultrastructure of dividing plant cell, xylem wall differentiation and distribution of cytoplasmic microtubules. Dev Biol 15:206–236CrossRefGoogle Scholar
  84. 84.
    Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20:744–749CrossRefGoogle Scholar
  85. 85.
    Prodham AKMA, Funada R, Ohtani J, Abe H, Fukazawa K (1995) Orientation of microfibrils and microtubules in developing tension-wood fibres of Japanese ash (Fraxinus mandshurica var.japonica). Planta 196:577–585Google Scholar
  86. 86.
    Qiu D, Wilson IW, Gan S, Washusen R, Moran GF, Southerton SG (2008) Gene expression in Eucalyptus branch wood with marked variation in cellulose microfibril orientation and lacking G-layers. New Phytol 179:94–103PubMedCrossRefGoogle Scholar
  87. 87.
    Rajangam AS, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P, Brown CJ, Hober S, Blomqvist K, Divne C, Ezcurra I, Mellerowicz E, Sundberg B, Bulone V, Teeri TT (2008) MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2, 6-dichlorobenzonitrile. Plant Physiol 148:1283–1294PubMedCrossRefGoogle Scholar
  88. 88.
    Roberts AW, Frost AO, Roberts EM, Haigler CH (2004) Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements. Protoplasma 224:217–229PubMedCrossRefGoogle Scholar
  89. 89.
    Roberts K, McCann MC (2000) Xylogenesis: the birth of a corpse. Curr Opin Plant Biol 3:517–522PubMedCrossRefGoogle Scholar
  90. 90.
    Roberts LW, Baba S (1968) IAA-induced xylem differentiation in the presence of colchicines. Plant Cell Physiol 9:315–321Google Scholar
  91. 91.
    Rojas M, Owen TP Jr, Lindahl KN (1999) Brefeldin A inhibits secondary cell wall synthesis in developing tracheary elements of Zinnia elegans. Int J Plant Sci 160:683–690CrossRefGoogle Scholar
  92. 92.
    Roll-Mecak A, McNally FJ (2010) Microtubule-severing enzymes. Curr Opin Cell Biol 22:96–103PubMedCrossRefGoogle Scholar
  93. 93.
    Salnikov VV, Grimson MJ, Delmer DP, Haigler CH (2001) Sucrose synthase localizes to cellulose synthesis sites in tracheary elements. Phytochemistry 57:823–833PubMedCrossRefGoogle Scholar
  94. 94.
    Sharma N, Bryant J, Wloga D, Donaldson R, Davis RC, Jerka-Dziadosz M, Gaertig J (2007) Katanin regulates dynamics of microtubules and biogenesis of motile cilia. J Cell Biol 178:1065–1079PubMedCrossRefGoogle Scholar
  95. 95.
    Smertenko AP, Chang HY, Wagner V, Kaloriti D, Fenyk S, Sonobe S, Lloyd C, Hauser MT, Hussey PJ (2004) The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 16:2035–2047PubMedCrossRefGoogle Scholar
  96. 96.
    Snustad DP, Haas NA, Kopczak SD, Silflow CD (1992) The small genome of Arabidopsis contains at least nine expressed beta-tubulin genes. Plant Cell 4:549–556PubMedCrossRefGoogle Scholar
  97. 97.
    Sonesson, A., Berglund, M., Staxén, I., Widell, S. 1997. The characterization of plasma membrane-bound tubulin of cauliflower using Triton X-114 fractionation. Plant Physiol. 115:1001–7.Google Scholar
  98. 98.
    Spokevicius AV, Southerton SG, MacMillan CP, Qiu D, Gan S, Tibbits JF, Moran GF, Bossinger G (2007) beta-tubulin affects cellulose microfibril orientation in plant secondary fibre cell walls. Plant J 51:717–726PubMedCrossRefGoogle Scholar
  99. 99.
    Thitamadee S, Tuchihara K, Hashimoto T (2002) Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417:193–196PubMedCrossRefGoogle Scholar
  100. 100.
    Turner S, Gallois P, Brown D (2007) Tracheary element differentiation. Annu Rev Plant Biol 58:407–433PubMedCrossRefGoogle Scholar
  101. 101.
    Uehara K, Hogetsu T (1993) Arrangement of cortical microtubules during formation of bordered pit in the tracheids of Taxus. Protoplasma 172:145–153CrossRefGoogle Scholar
  102. 102.
    Washusen R, Evans R, Southerton S (2005) A study of Eucalyptus grandis and Eucalyptus globulus branch wood microstructure. IAWA J 26:203–210Google Scholar
  103. 103.
    Wightman R, Marshall R, Turner SR (2009) A cellulose synthase-containing compartment moves rapidly beneath sites of secondary wall synthesis. Plant Cell Physiol 50:584–594PubMedCrossRefGoogle Scholar
  104. 104.
    Wightman R, Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54:794–805PubMedCrossRefGoogle Scholar
  105. 105.
    Wightman R, Turner SR (2010) Trafficking of the plant cellulose synthase complex. Plant Physiol 153:427–432PubMedCrossRefGoogle Scholar
  106. 106.
    Wightman R, Turner SR (2010) Trafficking of the cellulose synthase complex in developing xylem vessels. Biochem Soc Trans 38:755–760PubMedCrossRefGoogle Scholar
  107. 107.
    Ye ZH, Freshour G, Hahn MG, Burk DH, Zhong R (2002) Vascular development in Arabidopsis. Int Rev Cytol 220:225–256PubMedCrossRefGoogle Scholar
  108. 108.
    Yoshimura T, Demura T, Igarashi M, Fukuda H (1996) Differential expression of three genes for different β-tubulin isotypes during the initial culture of Zinnia mesophyll cells that divide and differentiate into tracheary elements. Plant Cell Physiol 37:1167–1176PubMedGoogle Scholar
  109. 109.
    Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers EP (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138:803–818PubMedCrossRefGoogle Scholar
  110. 110.
    Zhong R, Burk DH, Morrison WH, Ye ZH (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101–3117PubMedCrossRefGoogle Scholar
  111. 111.
    Zhou J, Qiu J, Ye ZH (2007) Alteration in secondary wall deposition by overexpression of the FRA1 kinesin-like protein in Arabidopsis. J Integr Plant Biol 49:1235–1243CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.John Innes CentreNorwichUK
  2. 2.Umeå Plant Science CentreUmeå UniversityUmeåSweden

Personalised recommendations