Advertisement

Microtubules in Plant Cells: Strategies and Methods for Immunofluorescence, Transmission Electron Microscopy, and Live Cell Imaging

  • Katherine Celler
  • Miki Fujita
  • Eiko Kawamura
  • Chris Ambrose
  • Klaus Herburger
  • Andreas Holzinger
  • Geoffrey O. Wasteneys
Part of the Methods in Molecular Biology book series (MIMB, volume 1365)

Abstract

Microtubules (MTs) are required throughout plant development for a wide variety of processes, and different strategies have evolved to visualize and analyze them. This chapter provides specific methods that can be used to analyze microtubule organization and dynamic properties in plant systems and summarizes the advantages and limitations for each technique. We outline basic methods for preparing samples for immunofluorescence labeling, including an enzyme-based permeabilization method, and a freeze-shattering method, which generates microfractures in the cell wall to provide antibodies access to cells in cuticle-laden aerial organs such as leaves. We discuss current options for live cell imaging of MTs with fluorescently tagged proteins (FPs), and provide chemical fixation, high-pressure freezing/freeze substitution, and post-fixation staining protocols for preserving MTs for transmission electron microscopy and tomography.

Key words

Microtubules EB1 GFP Kinesin MAP4 MBD MOR1 ARK1 Electron tomography Live cell imaging Correlative light and electron microscopy Immunofluorescence 

Notes

Acknowledgements

This chapter has been supported by Austrian Science Fund (FWF) project P24242-B16 to AH and funding from the Natural Sciences and Engineering Research Council and the Canadian Institutes of Health Research to GOW. The Thieme Verlag KG is acknowledged for their kind permission to reproduce Fig. 1b, c. Figure 6a–c is reproduced with permission of the National Academy of Sciences of the United States of America, and Dr. Jennifer Lippincott-Schwartz, National Institute of Child Health and Human Development, Bethesda, MD. Elsevier Inc. for reproduction of Fig. 10.

References

  1. 1.
    Rasmussen CG, Wright AJ, Muller S (2013) The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J 75(2):258–269. doi: 10.1111/tpj.12177 CrossRefPubMedGoogle Scholar
  2. 2.
    Louveaux M, Hamant O (2013) The mechanics behind cell division. Curr Opin Plant Biol 16(6):774–779. doi: 10.1016/j.pbi.2013.10.011 CrossRefPubMedGoogle Scholar
  3. 3.
    Masoud K, Herzog E, Chaboute ME, Schmit AC (2013) Microtubule nucleation and establishment of the mitotic spindle in vascular plant cells. Plant J 75(2):245–257. doi: 10.1111/tpj.12179 CrossRefPubMedGoogle Scholar
  4. 4.
    Ruan Y, Wasteneys GO (2014) CLASP: a microtubule-based integrator of the hormone-mediated transitions from cell division to elongation. Curr Opin Plant Biol 22:149–158. doi: 10.1016/j.pbi.2014.11.003 CrossRefPubMedGoogle Scholar
  5. 5.
    Ambrose C, Wasteneys GO (2011) Cell edges accumulate gamma tubulin complex components and nucleate microtubules following cytokinesis in Arabidopsis thaliana. PLoS One 6(11):e27423. doi: 10.1371/journal.pone.0027423 PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495. doi: 10.1126/science.1126551 CrossRefPubMedGoogle Scholar
  7. 7.
    Fujita M, Himmelspach R, Hocart CH, Williamson RE, Mansfield SD, Wasteneys GO (2011) Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis. Plant J 66(6):915–928. doi: 10.1111/j.1365-313X.2011.04552.x CrossRefPubMedGoogle Scholar
  8. 8.
    Lei L, Li SD, Bashline L, Gu Y (2014) Dissecting the molecular mechanism underlying the intimate relationship between cellulose microfibrils and cortical microtubules. Front Plant Sci 5:8. doi: 10.3389/fpls.2014.00090 CrossRefGoogle Scholar
  9. 9.
    Fujita M, Lechner B, Barton DA, Overall RL, Wasteneys GO (2012) The missing link: do cortical microtubules define plasma membrane nanodomains that modulate cellulose biosynthesis? Protoplasma 249:S59–S67. doi: 10.1007/s00709-011-0332-z CrossRefPubMedGoogle Scholar
  10. 10.
    Oda Y, Fukuda H (2013) The dynamic interplay of plasma membrane domains and cortical microtubules in secondary cell wall patterning. Front Plant Sci 4:6. doi: 10.3389/fpls.2013.00511 CrossRefGoogle Scholar
  11. 11.
    Sampathkumar A, Yan A, Krupinski P, Meyerowitz EM (2014) Physical forces regulate plant development and morphogenesis. Curr Biol 24(10):R475–R483. doi: 10.1016/j.cub.2014.03.014 PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Ivakov A, Persson S (2013) Plant cell shape: modulators and measurements. Front Plant Sci 4:13. doi: 10.3389/fpls.2013.00439 CrossRefGoogle Scholar
  13. 13.
    Zhang CH, Halsey LE, Szymanski DB (2011) The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol 11:13. doi: 10.1186/1471-2229-11-27 CrossRefGoogle Scholar
  14. 14.
    Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17(6):657–665. doi: 10.1046/j.1365-313X.1999.00415.x CrossRefPubMedGoogle Scholar
  15. 15.
    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(1):157–171. doi: 10.1111/j.1365-313X.2007.03327.x CrossRefPubMedGoogle Scholar
  16. 16.
    Sieberer B, Timmers A (2009) Microtubules in plant root hairs and their role in cell polarity and tip growth in root hairs. In: Emons A, Ketelaar T (eds) Plant cell monograph, vol 12. Springer, Berlin, pp 233–248Google Scholar
  17. 17.
    Ambrose C, Wasteneys GO (2014) Microtubule initiation from the nuclear surface controls cortical microtubule growth polarity and orientation in Arabidopsis thaliana. Plant Cell Physiol 55(9):1636–1645. doi: 10.1093/pcp/pcu094 PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64:243–265. doi: 10.1146/annurev-arplant-050312-120150 CrossRefPubMedGoogle Scholar
  19. 19.
    Chebli Y, Kroeger J, Geitmann A (2013) Transport logistics in pollen tubes. Mol Plant 6(4):1037–1052. doi: 10.1093/mp/sst073 CrossRefPubMedGoogle Scholar
  20. 20.
    Yu R, Huang RF, Wang XC, Yuan M (2001) Microtubule dynamics are involved in stomatal movement of Vicia faba L. Protoplasma 216(1-2):113–118. doi: 10.1007/Bf02680138 CrossRefPubMedGoogle Scholar
  21. 21.
    Brandizzi F, Wasteneys GO (2013) Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J 75(2):339–349. doi: 10.1111/tpj.12227 CrossRefPubMedGoogle Scholar
  22. 22.
    Foissner I, Menzel D, Wasteneys GO (2009) Microtubule-dependent motility and orientation of the cortical endoplasmic reticulum in elongating characean internodal cells. Cell Motil Cytoskeleton 66(3):142–155. doi: 10.1002/Cm.20337 CrossRefPubMedGoogle Scholar
  23. 23.
    Hamada T, Ueda H, Kawase T, Hara-Nishimura I (2014) Microtubules contribute to tubule elongation and anchoring of endoplasmic reticulum, resulting in high network complexity in Arabidopsis. Plant Physiol 166(4):1869–1876. doi: 10.1104/pp. 114.252320 PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Holzinger A, Lütz-Meindl U (2002) Kinesin-like proteins are involved in postmitotic nuclear migration of the unicellular green alga Micrasterias denticulata. Cell Biol Int 26(8):689–697. doi: 10.1006/cbir.2002.0920 CrossRefPubMedGoogle Scholar
  25. 25.
    Holzinger A, Lütz-Meindl U (2003) Evidence for kinesin- and dynein-like protein function in circular nuclear migration in the green alga Pleurenterium tumidum: digital time lapse analysis of inhibitor effects. J Phycol 39(1):106–114. doi: 10.1046/j.1529-8817.2003.02074.x CrossRefGoogle Scholar
  26. 26.
    Miki T, Nishina M, Goshima G (2015) RNAi screening identifies the armadillo repeat-containing kinesins responsible for microtubule-dependent nuclear positioning in Physcomitrella patens. Plant Cell Physiol 56:737. doi: 10.1093/pcp/pcv002 CrossRefPubMedGoogle Scholar
  27. 27.
    Tatout C, Evans DE, Vanrobays E, Probst AV, Graumann K (2014) The plant LINC complex at the nuclear envelope. Chromosome Res 22(2):241–252. doi: 10.1007/s10577-014-9419-7 CrossRefPubMedGoogle Scholar
  28. 28.
    Kandasamy MK, Meagher RB (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskeleton 44(2):110–118. doi: 10.1002/(Sici)1097-0169(199910)44:2<110::Aid-Cm3>3.0.Co;2-O CrossRefPubMedGoogle Scholar
  29. 29.
    Holzinger A, Wasteneys GO, Lütz C (2007) Investigating cytoskeletal function in chloroplast protrusion formation in the arctic-alpine plant Oxyria digyna. Plant Biol 9(3):400–410. doi: 10.1055/s-2006-924727 CrossRefPubMedGoogle Scholar
  30. 30.
    Holzinger A, Kwok EY, Hanson MR (2008) Effects of arc3, arc5 and arc6 mutations on plastid morphology and stromule formation in green and nongreen tissues of Arabidopsis thaliana. Photochem Photobiol 84(6):1324–1335. doi: 10.1111/j.1751-1097.2008.00437.x CrossRefPubMedGoogle Scholar
  31. 31.
    Zaffryar S, Zimerman B, Abu-Abied M, Belausov E, Lurya G, Vainstein A, Kamenetsky R, Sadot E (2007) Development-specific association of amyloplasts with microtubules in scale cells of Narcissus tazetta. Protoplasma 230(3-4):153–163. doi: 10.1007/s00709-006-0238-3 CrossRefPubMedGoogle Scholar
  32. 32.
    Gilroy S (1997) Fluorescence microscopy of living plant cells. Annu Rev Plant Physiol Plant Mol Biol 48:165–190. doi: 10.1146/annurev.arplant.48.1.165 CrossRefPubMedGoogle Scholar
  33. 33.
    Mathur J (2007) The illuminated plant cell. Trends Plant Sci 12(11):506–513. doi: 10.1016/j.tplants.2007.08.017 CrossRefPubMedGoogle Scholar
  34. 34.
    Dixit R, Cyr R, Gilroy S (2006) Using intrinsically fluorescent proteins for plant cell imaging. Plant J 45(4):599–615. doi: 10.1111/j.1365-313X.2006.02658.x CrossRefPubMedGoogle Scholar
  35. 35.
    Wasteneys GO, WillingaleTheune J, Menzel D (1997) Freeze shattering: a simple and effective method for permeabilizing higher plant cell walls. J Microsc 188:51–61. doi: 10.1046/j.1365-2818.1977.2390796.x CrossRefPubMedGoogle Scholar
  36. 36.
    Kwok EY, Hanson MR (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J 35(1):16–26. doi: 10.1046/j.1365-313X.2003.01777.x CrossRefPubMedGoogle Scholar
  37. 37.
    Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300(5626):1715–1718. doi: 10.1126/science.1083529 CrossRefPubMedGoogle Scholar
  38. 38.
    Chan J, Calder G, Fox S, Lloyd C (2007) Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 9(2):171–U157. doi: 10.1038/Ncb1533 CrossRefPubMedGoogle Scholar
  39. 39.
    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(24):4114–4123. doi: 10.1242/Jcs.039065 CrossRefPubMedGoogle Scholar
  40. 40.
    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(1):102–114. doi: 10.1104/pp. 105.069989 PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, Evrard JL, Schmit AC, Guerche P, Bouchez D (2006) gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18(6):1412–1425. doi: 10.1105/039644 PubMedCentralCrossRefPubMedGoogle Scholar
  42. 42.
    Chang HY, Smertenko AP, Igarashi H, Dixon DP, Hussey PJ (2005) Dynamic interaction of NtMAP65-1a with microtubules in vivo. J Cell Sci 118(14):3195–3201. doi: 10.1242/Jcs.02433 CrossRefPubMedGoogle Scholar
  43. 43.
    Shaw SL (2006) Imaging the live plant cell. Plant J 45(4):573–598. doi: 10.1111/j.1365-313X.2006.02653.x CrossRefPubMedGoogle Scholar
  44. 44.
    Hell SW (2003) Toward fluorescence nanoscopy. Nat Biotechnol 21(11):1347–1355. doi: 10.1038/nbt895 CrossRefPubMedGoogle Scholar
  45. 45.
    Dyba M, Jakobs S, Hell SW (2003) Immunofluorescence stimulated emission depletion microscopy. Nat Biotechnol 21(11):1303–1304. doi: 10.1038/nbt897 CrossRefPubMedGoogle Scholar
  46. 46.
    Hell SW (2007) Far-field optical nanoscopy. Science 316(5828):1153–1158. doi: 10.1126/science.1137395 CrossRefPubMedGoogle Scholar
  47. 47.
    Folling J, Bossi M, Bock H, Medda R, Wurm CA, Hein B, Jakobs S, Eggeling C, Hell SW (2008) Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods 5(11):943–945. doi: 10.1038/nmeth.1257 CrossRefPubMedGoogle Scholar
  48. 48.
    Balint S, Verdeny Vilanova I, Sandoval Alvarez A, Lakadamyali M (2013) Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections. Proc Natl Acad Sci U S A 110(9):3375–3380. doi: 10.1073/pnas.1219206110 PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM, Manley S, Sougrat R, Waterman CM, Kanchanawong P, Davidson MW, Fetter RD, Hess HF (2009) Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc Natl Acad Sci U S A 106(9):3125–3130. doi: 10.1073/pnas.0813131106 PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Komis G, Mistrik M, Samajova O, Doskocilova A, Ovecka M, Illes P, Bartek J, Samaj J (2014) Dynamics and organization of cortical microtubules as revealed by superresolution structured illumination microscopy. Plant Physiol 165(1):129–148. doi: 10.1104/pp. 114.238477 PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Ledbetter MC, Porter KR (1963) A microtubule in plant cell fine structure. J Cell Biol 19(1):239. doi: 10.1083/Jcb.19.1.239 PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Meindl U, Lancelle S, Hepler PK (1992) Vesicle production and fusion during lobe formation in Micrasterias Visualized by high-pressure freeze fixation. Protoplasma 170(3-4):104–114. doi: 10.1007/Bf01378786 CrossRefGoogle Scholar
  53. 53.
    Holzinger A (2000) Aspects of cell development in Micrasterias muricata (Desmidiaceae) revealed by cryofixation and freeze substitution. Nova Hedwigia 70(3-4):275–287Google Scholar
  54. 54.
    Segui-Simarro JM, Austin JR, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16(4):836–856. doi: 10.1105/Tpc.017749 PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Eder M, Lutz-Meindl U (2008) Pectin-like carbohydrates in the green alga Micrasterias characterized by cytochemical analysis and energy filtering TEM. J Microsc 231(2):201–214. doi: 10.1111/j.1365-2818.2008.02036.x CrossRefPubMedGoogle Scholar
  56. 56.
    Holzinger A, Valenta R, Lutz-Meindl U (2000) Profilin is localized in the nucleus-associated microtubule and actin system and is evenly distributed in the cytoplasm of the green alga Micrasterias denticulata. Protoplasma 212(3-4):197–205. doi: 10.1007/Bf01282920 CrossRefGoogle Scholar
  57. 57.
    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(10):4534–4544. doi: 10.1091/mbc.E08-04-0341 PubMedCentralCrossRefPubMedGoogle Scholar
  58. 58.
    Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45(9):1330–1334. doi: 10.1093/Pcp/Pch300 CrossRefPubMedGoogle Scholar
  59. 59.
    Holzinger A, Karsten U, Lutz C, Wiencke C (2006) Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa from Spitsbergen (Norway) under UV exposure. Phycologia 45(2):168–177. doi: 10.2216/05-20.1 CrossRefGoogle Scholar
  60. 60.
    Ambrose C, Allard JF, Cytrynbaum EN, Wasteneys GO (2011) A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat Commun 2:430. doi: 10.1038/ncomms1444 PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124(4):1493–1506PubMedCentralCrossRefPubMedGoogle Scholar
  62. 62.
    Frank J (2006) Electron tomography methods for three-dimensional visualization of structures in the cell. Springer, New York, NYGoogle Scholar
  63. 63.
    Nitta K, Kaneko Y (2004) Simple plunge freezing applied to plant tissues for capturing the ultrastructure close to the living state. J Electron Microsc (Tokyo) 53(6):677–680. doi: 10.1093/jmicro/dfh092 CrossRefGoogle Scholar
  64. 64.
    Koning RI, Celler K, Willemse J, Bos E, van Wezel GP, Koster AJ (2014) Correlative cryo-fluorescence light microscopy and cryo-electron tomography of Streptomyces. Methods Cell Biol 124:217–239. doi: 10.1016/B978-0-12-801075-4.00010-0 CrossRefPubMedGoogle Scholar
  65. 65.
    Ueda K, Matsuyama T, Hashimoto T (1999) Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206(1-3):201–206. doi: 10.1007/Bf01279267 CrossRefGoogle Scholar
  66. 66.
    Abe T, Hashimoto T (2005) Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43(2):191–204. doi: 10.1111/j.1365-313X.2005.02442.x CrossRefPubMedGoogle Scholar
  67. 67.
    Ambrose JC, Wasteneys GO (2008) CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Mol Biol Cell 19(11):4730–4737. doi: 10.1091/mbc.E08-06-0665 PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Granger CL, Cyr RJ (2001) Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP-MBD. Protoplasma 216(3-4):201–214CrossRefPubMedGoogle Scholar
  69. 69.
    Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136(4):3905–3919. doi: 10.1104/pp. 103.031591 PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17(3):1298–1305. doi: 10.1091/mbc.E05-09-0864 PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Littlejohn GR, Gouveia JD, Edner C, Smirnoff N, Love J (2010) Perfluorodecalin enhances in vivo confocal microscopy resolution of Arabidopsis thaliana mesophyll. New Phytol 186(4):1018–1025. doi: 10.1111/j.1469-8137.2010.03244.x CrossRefPubMedGoogle Scholar
  72. 72.
    Littlejohn GR, Love J (2012) A simple method for imaging Arabidopsis leaves using perfluorodecalin as an infiltrative imaging medium. J Vis Exp (59). doi: 10.3791/3394
  73. 73.
    Littlejohn GR, Mansfield JC, Christmas JT, Witterick E, Fricker MD, Grant MR, Smirnoff N, Everson RM, Moger J, Love J (2014) An update: improvements in imaging perfluorocarbon-mounted plant leaves with implications for studies of plant pathology, physiology, development and cell biology. Front Plant Sci 5:140. doi: 10.3389/fpls.2014.00140 PubMedCentralPubMedGoogle Scholar
  74. 74.
    Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26(1):31–43CrossRefPubMedGoogle Scholar
  75. 75.
    Sambade A, Pratap A, Buschmann H, Morris RJ, Lloyd C (2012) The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. Plant Cell 24(1):192–201. doi: 10.1105/tpc.111.093849 PubMedCentralCrossRefPubMedGoogle Scholar
  76. 76.
    Vineyard L, Elliott A, Dhingra S, Lucas JR, Shaw SL (2013) Progressive transverse microtubule array organization in hormone-induced Arabidopsis hypocotyl cells. Plant Cell 25(2):662–676. doi: 10.1105/tpc.112.107326 PubMedCentralCrossRefPubMedGoogle Scholar
  77. 77.
    Dixit R, Cyr R (2003) Cell damage and reactive oxygen species production induced by fluorescence microscopy: effect on mitosis and guidelines for non-invasive fluorescence microscopy. Plant J 36(2):280–290. doi: 10.1046/j.1365-313X.2003.01868.x CrossRefPubMedGoogle Scholar
  78. 78.
    Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5(11):967–971. doi: 10.1038/Ncb1057 CrossRefPubMedGoogle Scholar
  79. 79.
    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(22):1991–1997. doi: 10.1016/j.cub.2003.10.033 CrossRefPubMedGoogle Scholar
  80. 80.
    Marc J, Granger CL, Brincat J, Fisher DD, Kao TH, McCubbin AG, Cyr RJ (1998) A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10(11):1927–1939PubMedCentralPubMedGoogle Scholar
  81. 81.
    DeBolt S, Gutierrez R, Ehrhardt DW, Melo CV, Ross L, Cutler SR, Somerville C, Bonetta D (2007) Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proc Natl Acad Sci U S A 104(14):5854–5859. doi: 10.1073/pnas.0700789104 PubMedCentralCrossRefPubMedGoogle Scholar
  82. 82.
    Stoppin-Mellet V, Gaillard J, Vantard M (2006) Katanin’s severing activity favors bundling of cortical microtubules in plants. Plant J 46(6):1009–1017. doi: 10.1111/j.1365-313X.2006.02761.x CrossRefPubMedGoogle Scholar
  83. 83.
    Wightman R, Turner SR (2007) Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J 52(4):742–751. doi: 10.1111/j.1365-313X.2007.03271.x CrossRefPubMedGoogle Scholar
  84. 84.
    Holzinger A, Meindl U (1997) Jasplakinolide, a novel actin targeting peptide, inhibits cell growth and induces actin filament polymerization in the green alga Micrasterias. Cell Motil Cytoskeleton 38(4):365–372. doi: 10.1002/(Sici)1097-0169(1997)38:4<365::Aid-Cm6>3.0.Co;2-2 CrossRefPubMedGoogle Scholar
  85. 85.
    Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Salamin LM, Norlen LP, Richter K, Blanc NS, Studer D, Dubochet J (2004) Cryo-electron microscopy of vitreous sections. EMBO J 23(18):3583–3588. doi: 10.1038/sj.emboj.7600366 PubMedCentralCrossRefPubMedGoogle Scholar
  86. 86.
    Buser C, Walther P (2008) Freeze-substitution: the addition of water to polar solvents enhances the retention of structure and acts at temperatures around -60 degrees C. J Microsc 230(Pt 2):268–277. doi: 10.1111/j.1365-2818.2008.01984.x CrossRefPubMedGoogle Scholar
  87. 87.
    Walther P, Ziegler A (2002) Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208:3–10. doi: 10.1046/j.1365-2818.2002.01064.x CrossRefPubMedGoogle Scholar
  88. 88.
    Watanabe S, Punge A, Hollopeter G, Willig KI, Hobson RJ, Davis MW, Hell SW, Jorgensen EM (2011) Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 8(1):80–84. doi: 10.1038/nmeth.1537 PubMedCentralCrossRefPubMedGoogle Scholar
  89. 89.
    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):797–806. doi: 10.1038/ncb1886 CrossRefPubMedGoogle Scholar
  90. 90.
    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):1141–1154. doi: 10.1105/tpc.108.065334 PubMedCentralCrossRefPubMedGoogle Scholar
  91. 91.
    Eng RC, Wasteneys GO (2014) The microtubule plus-end tracking protein ARMADILLO-REPEAT KINESIN1 promotes microtubule catastrophe in Arabidopsis. Plant Cell 26(8):3372–3386. doi: 10.1105/tpc.114.126789 PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Katherine Celler
    • 1
  • Miki Fujita
    • 1
  • Eiko Kawamura
    • 2
  • Chris Ambrose
    • 3
  • Klaus Herburger
    • 4
  • Andreas Holzinger
    • 4
  • Geoffrey O. Wasteneys
    • 1
  1. 1.Department of BotanyThe University of British ColumbiaVancouverCanada
  2. 2.Western College of Veterinary MedicineUniversity of SaskatchewanSaskatoonCanada
  3. 3.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  4. 4.Functional Plant Biology, Institute of BotanyUniversity of InnsbruckInnsbruckAustria

Personalised recommendations