Straighten up and fly right-microtubule dynamics and organization of non-centrosomal arrays in higher plants

Current Opinion in Cell Biology

Volumn 20, Issue 1, 2008, Pages 107-116

  Ehrhardt, David W ^a  

^a GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; RNA;

CELL MIGRATION; CENTROSOME; HIGHER PLANT; IN VITRO STUDY; IN VIVO STUDY; MICROTUBULE; NONHUMAN; PLANT CELL; POLYMERIZATION; PRIORITY JOURNAL; REVIEW;

CENTROSOME; MICROTUBULES; PLANTS;

EMBRYOPHYTA;

EID: 39149087966     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2007.12.004     Document Type: Review

References (69)

1. Doxsey S., McCollum D., and Theurkauf W. Centrosomes in cellular regulation. Annu Rev Cell Dev Biol 21 (2005) 411-434
2. Mitchison T., and Kirschner M. Dynamic instability of microtubule growth. Nature 312 (1984) 237-242
3. Gundersen G.G., Gomes E.R., and Wen Y. Cortical control of microtubule stability and polarization. Curr Opin Cell Biol 16 (2004) 106-112
4. Luders J., and Stearns T. Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8 (2007) 161-167
5. Bartolini F., and Gundersen G.G. Generation of noncentrosomal microtubule arrays. J Cell Sci 119 (2006) 4155-4163
6. Paradez A., Wright A., and Ehrhardt D.W. Microtubule cortical array organization and plant cell morphogenesis. Curr Opin Plant Biol 9 (2006) 571-578
7. Mazia D. Centrosomes and mitotic poles. Exp Cell Res 153 (1984) 1-15
8. Ehrhardt D.W., and Shaw S.L. Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57 (2006) 859-875
9. Murata M., Sonobe S., Baskin T.I., Hyodo S., Hasezawa S., Nagata T., Horio T., and Hasebe M. Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol 10 (2005) 961-968
10. Chan J., Calder G., Doonan J., and Lloyd C. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5 (2003) 967-971
11. Shaw S., Kamyar R., and Ehrhardt D. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300 (2003) 1715-1718
12. Pastuglia M., Azimzadeh J., Goussot M., Camilleri C., Belcram K., Evrard J.L., Schmit A.C., Guerche P., and Bouchez D. Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18 (2006) 1412-1425. Gamma-tubulin is encoded by two functionally redundant genes in Arabidopsis. To assess function, double mutants were constructed with both strong alleles at both loci and with combination of strong and weak alleles. Analysis of these double mutants revealed that gamma tubulin is an essential protein for formation of all major MT arrays in Arabidopsis and their function in carrying out cell division and cell morphogenesis.
13. •], RNAi knockdown of gamma tubulin in Arabidopsis reveals that gamma tubulin is essential for all major MT arrays, cell morphogenesis and cell division. In a series of RNAi plants, sensitivity to loss of gamma tubulin function in specific developmental pathways is observed, such as stomatal patterning.
14. Erhardt M., Stoppin-Mellet V., Campagne S., Canaday J., Mutterer J., Fabian T., Sauter M., Muller T., Peter C., Lambert A.M., et al. The plant Spc98p homologue colocalizes with gamma-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115 (2002) 2423-2431
15. Seltzer V., Janski N., Canaday J., Herzog E., Erhardt M., Evrard J.L., and Schmit A.C. Arabidopsis GCP2 and GCP3 are part of a soluble gamma-tubulin complex and have nuclear envelope targeting domains. Plant J 52 (2007) 322-331
16. Van Damme D., Van Poucke K., Boutant E., Ritzenthaler C., Inze D., and Geelen D. In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136 (2004) 3956-3967
17. Cai G., Ovidi E., Romagnoli S., Vantard M., Cresti M., and Tiezzi A. Identification and characterization of plasma membrane proteins that bind to microtubules in pollen tubes and generative cells of tobacco. Plant Cell Physiol 46 (2005) 563-578
18. Buschmann H., Fabri C.O., Hauptmann M., Hutzler P., Laux T., Lloyd C.W., and Schaffner A.R. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol 14 (2004) 1515-1521
19. Walker K.L., Muller S., Moss D., Ehrhardt D.W., and Smith L.G. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17 (2007) 1827-1836. The Arabidopsis TANGLED protein is shown to be recruited to the preprophase band and to remain as an annulus at the cell cortex throughout mitosis and cytokinesis. Together with genetic evidence that TANGLED is required for phragmoplast guidance during cytokinesis, these data suggest that TANGLED is an excellent candidate for a cortical cue that marks and remembers the division site after PPB disassembly.
20. Gardiner J., Harper J., Weerakoon N., Collings D., Ritchie S., Gilroy S., Cyr R., and Marc J. A 90-kDa phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13 (2001) 2143-2158
21. Dhonukshe P., Laxalt A., Goedhart J., Gadella T., and Munnik T. Phospholipase d activation correlates with microtubule reorganization in living plant cells. Plant Cell 15 (2003) 2666-2679
22. DeBolt S., Gutierrez R., Ehrhardt D.W., Melo C.V., Ross L., Cutler S.R., Somerville C., and Bonetta D. Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proc Natl Acad Sci U S A 104 (2007) 5854-5859. A small molecule inhibitor of both microtubule dynamics and cellulose synthase is described. Morlin, a coumarin, inhibits both polymer growth and polymer shrinking, suggesting that it inhibits a facilitator of both dimer gain and loss.
23. Hirase A., Hamada T., Itoh T.J., Shimmen T., and Sonobe S. n-Butanol induces depolymerization of microtubules in vivo and in vitro. Plant Cell Physiol 47 (2006) 1004-1009
24. Chu Z., Chen H., Zhang Y., Zhang Z., Zheng N., Yin B., Yan H., Zhu L., Zhao X., Yuan M., et al. Knockout of the AtCESA2 gene affects microtubule orientation and causes abnormal cell expansion in Arabidopsis. Plant Physiol 143 (2007) 213-224
25. Paredez A.R., Somerville C.R., and Ehrhardt D.W. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312 (2006) 1491-1495. Imaging of a functional cellulose synthase isozyme tagged with a fluorescent protein permits direct visualization of cellulose synthase complexes in living cells for the first time. The trajectories of CESA complexes in the plasma membrane as they synthesize cellulose are shown to be organized and guided by individual elements of the cortical microtubule array.
26. Nguema-Ona E., Bannigan A., Chevalier L., Baskin T.I., and Driouich A. Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana. Plant J 52 (2007) 240-251. Treatment of roots with both Yariv reagent and monoclonal antibodies directed against arabinogalatan proteins is shown to disrupt cortical MT organization as visualized both with immunocytochemistry and GFP-tagged microtubules. These results suggest that AGP function in the apoplast may feed back on microtubule organization in the cell cortex.
27. Sardar H.S., Yang J., and Showalter A.M. Molecular interactions of arabinogalactan proteins with cortical microtubules and F-actin in Bright Yellow-2 tobacco cultured cells. Plant Physiol 142 (2006) 1469-1479. Experiments with Yariv reagent and cytoskeletal disrupting drugs suggest that arabinogalactan proteins may be required for normal cortical cytoskeletal organization, and in turn, cytoskeletal organization may be required for AGP localization.
28. Sedbrook J.C. MAPs in plant cells: delineating microtubule growth dynamics and organization. Curr Opin Plant Biol 7 (2004) 632-640
29. Ambrose J.C., Shoji T., Kotzer A.M., Pighin J.A., and Wasteneys G.O. The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19 (2007) 2763-2775. CLASP, a +TIP protein conserved among plants and animals is shown to be required for cell division and anisotropic cell growth in Arabidopsis.
30. Kirik V., Herrmann U., Parupalli C., Sedbrook J.C., Ehrhardt D.W., and Hulskamp M. CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis. J Cell Sci (2007). The Arabidopsis CLASP protein is shown to localize to a domain just behind EB1b at the plus ends of cortical microtubules and also to prominent spots distributed along the microtubule lattice. This latter localization pattern appears to be a feature of cortical microtubules and is not evident in the spindle or phragmoplast arrays. The authors speculate that CLASP might play a special role in addition to plus end function at the cell cortex.
31. Nakajima K., Furutani I., Tachimoto H., Matsubara H., and Hashimoto T. SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16 (2004) 1178-1190
32. Sedbrook J.C., Ehrhardt D.W., Fisher S.E., Scheible W.R., and Somerville C.R. The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16 (2004) 1506-1520
33. Nakajima K., Kawamura T., and Hashimoto T. Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol 47 (2006) 513-522. While loss-of-function alleles of the spr1 locus primarily cause spiral growth of cell files and plant organs, coincident with a change in pitch of the cortical cytoskeletal array, crosses made with mutants in other members of the gene family cause severe loss of anisotropic cell growth and general loss of cortical array organization, suggesting that the gene family is partially redundant in function and essential for cytoskeletal organization and function.
34. Furutani I., Watanabe Y., Prieto R., Masukawa M., Suzuki K., Naoi K., Thitamadee S., Shikanai T., and Hashimoto T. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127 (2000) 4443-4453
35. Lansbergen G., Grigoriev I., Mimori-Kiyosue Y., Ohtsuka T., Higa S., Kitajima I., Demmers J., Galjart N., Houtsmuller A.B., Grosveld F., et al. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev Cell 11 (2006) 21-32
36. Stoppin-Mellet V., Gaillard J., and Vantard M. Katanin's severing activity favors bundling of cortical microtubules in plants. Plant J 46 (2006) 1009-1017. The katanin P60 catalytic subunit has been a hot spot for mutants that affect plant cell and organ cell growth. In this study, an inducible construct is used to overexpress P60 in Arabidopsis cells in order determine how gain of Katanin activity affects cytoskeletal organization. As expected, the length distribution of cortical microtubules is eventually diminished, and overall array ordering is lost. Somewhat surprisingly, prominent polymer bundles are formed during the transition.
37. Dhonukshe P., Bargmann B.O., and Gadella Jr. T.W. Arabidopsis tubulin folding cofactor B interacts with alpha-tubulin in vivo. Plant Cell Physiol 47 (2006) 1406-1411
38. Kirik V., Mathur J., Grini P.E., Klinkhammer I., Adler K., Bechtold N., Herzog M., Bonneville J.M., and Hulskamp M. Functional analysis of the tubulin-folding cofactor C in Arabidopsis thaliana. Curr Biol 12 (2002) 1519-1523
39. Kirik V., Grini P.E., Mathur J., Klinkhammer I., Adler K., Bechtold N., Herzog M., Bonneville J.M., and Hulskamp M. The Arabidopsis TUBULIN-FOLDING COFACTOR A gene is involved in the control of the alpha/beta-tubulin monomer balance. Plant Cell 14 (2002) 2265-2276
40. Steinborn K., Maulbetsch C., Priester B., Trautmann S., Pacher T., Geiges B., Kuttner F., Lepiniec L., Stierhof Y.D., Schwarz H., et al. The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev 16 (2002) 959-971
41. Whittington A.T., Vugrek O., Wei K.J., Hasenbein N.G., Sugimoto K., Rashbrooke M.C., and Wasteneys G.O. MOR1 is essential for organizing cortical microtubules in plants. Nature 411 (2001) 610-613
42. Li H., Yuan M., and Mao T. AtMAP65-1 binds to tubulin dimers to promote tubulin assembly. J Biochem Mol Biol 40 (2007) 218-225
43. Wang X., Zhu L., Liu B., Wang C., Jin L., Zhao Q., and Yuan M. Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19 (2007) 877-889. A novel MAP is reported and shown to be required for normal organ axis growth pattern and for morphogenesis of many cell types. MAP18 inhibits tubulin polymerization in vitro, and plants overexpressing MAP18 are hypersensitive to MT destabilizing drugs, suggesting that MAP18 acts to destabilize microtubules in vivo.
44. Perrin R.M., Wang Y., Yuen C.Y., Will J., and Masson P.H. WVD2 is a novel microtubule-associated protein in Arabidopsis thaliana. Plant J 49 (2007) 961-971. The wvd2 locus is shown to encode a novel MAP that is required for cell morphogenesis. Loss of WVD2 function causes a reduction in MT-bundling events mediated by polymer treadmilling.
45. Korolev A.V., Buschmann H., Doonan J.H., and Lloyd C.W. 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 (2007) 2241-2247. MAP70-5, is shown to be a novel MAP and to be required for normal cell morphogenesis and growth pattern of the plant axis. MAP70-5 causes development of ectopic poles of cell growth when overexpressed in vivo and increases the length distribution of microtubules in vitro, suggesting that it acts to stabilize microtubule growth.
46. Dixit R., and Cyr R. Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16 (2004) 3274-3284
47. Dixit R., Chang E., and Cyr R. Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17 (2006) 1298-1305. Anaylsis of EB1-GFP labeled microtubules in tobacco tissue culture cells and Arabidosis plants reveals evidence for a bias in the polarity of cortical microtubules in large cellular domains. Domains of differing net polarity may exist side by side in individual cells.
48. Chan J., Calder G., Fox S., and Lloyd C. Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 9 (2007) 171-175
49. Chan J., Jensen C.G., Jensen L.C., Bush M., and Lloyd C.W. The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci U S A 96 (1999) 14931-14936. Long-term imaging of cortical arrays in the Arabidopsis hypocotyl confirms a previous study that suggested some cortical arrays may undergo independent rotation and reveals that these rotating movements are caused by fields of co-oriented microtubules migrating across the cell cortex.
50. Smertenko A., Saleh N., Igarashi H., Mori H., Hauser-Hahn I., Jiang C.J., Sonobe S., Lloyd C.W., and Hussey P.J. A new class of microtubule-associated proteins in plants. Nat Cell Biol 2 (2000) 750-753
51. Wicker-Planquart C., Stoppin-Mellet V., Blanchoin L., and Vantard M. Interactions of tobacco microtubule-associated protein MAP65-1b with microtubules. Plant J 39 (2004) 126-134
52. Smertenko A.P., Chang H.Y., Wagner V., Kaloriti D., Fenyk S., Sonobe S., Lloyd C., Hauser M.T., and Hussey P.J. The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 16 (2004) 2035-2047
53. Chang H.Y., Smertenko A.P., Igarashi H., Dixon D.P., and Hussey P.J. Dynamic interaction of NtMAP65-1a with microtubules in vivo. J Cell Sci 118 (2005) 3195-3201
54. Mao T., Jin L., Li H., Liu B., and Yuan M. Two microtubule-associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiol 138 (2005) 654-662
55. Li H., Mao T., Zhang Z., and Yuan M. The AtMAP65-1 cross-bridge between microtubules is formed by one dimer. Plant Cell Physiol 48 (2007) 866-874. In vitro studies of MAP65-1 peptides support a model where the N-terminal domain of MAP65-1 forms the 25 nm cross-bridge between MT lattices as a dimer, and the C-terminal domain acts as the MT binding surface.
56. Smertenko A.P., Chang H.Y., Sonobe S., Fenyk S.I., Weingartner M., Bogre L., and Hussey P.J. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 119 (2006) 3227-3237. MAP65-1 is shown to be hyper-phosphorylated in a cell cycle dependent fashion, with CDK and MAP being two likely kinases. Phosphorylation inhibits MAP65-1 activity, and phosphomimics of candidate phosphorylation sites confirms that these sites are required for regulation of MT interaction in vitro and in vivo and for mitotic spindle function.
57. Sasabe M., Soyano T., Takahashi Y., Sonobe S., Igarashi H., Itoh T.J., Hidaka M., and Machida Y. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 20 (2006) 1004-1014. Tobacco MAP65-1 is shown to be phosphorylated by the tobacco MAPK NRF1/NTF6 in a cell cycle dependent fashion. The phosphorylated protein accumulates that phragmoplast equator and is reduced in its MT-bundling activity. Overexpression of a non-phosphorylatable form of MAP65-1 delays phragmoplast expansion, suggesting that downregulation of MAP65-1-bundling activity may be needed to support phragmoplast development.
58. Loiodice I., Staub J., Setty T.G., Nguyen N.P., Paoletti A., and Tran P.T. Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol Biol Cell 16 (2005) 1756-1768
59. Wightman R., and Turner S.R. Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J (2007). Imaging of treadmilling cortical microtubules reveals that most severing events occur coincident with the position of MT-MT cross-overs. This behavior has the potential to be a biasing mechanism in ordering the cortical array.
60. Shoji T., Narita N.N., Hayashi K., Asada J., Hamada T., Sonobe S., Nakajima K., and Hashimoto T. Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol 136 (2004) 3933-3944
61. Naoi K., and Hashimoto T. A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization. Plant Cell 16 (2004) 1841-1853
62. Abe T., Thitamadee S., and Hashimoto T. Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol 45 (2004) 211-220
63. Ishida T., Kaneko Y., Iwano M., and Hashimoto T. Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc Natl Acad Sci U S A 104 (2007) 8544-8549. Analysis of a large collection of spiral growth mutants shows a marked inverse correlation between cortical array pitch and handedness and spiral growth pitch and handedness. In addition, genetic evidence suggests that GTP-hydrolysis is a determinant of EB1 association with the MT lattice.
64. Thitamadee S., Tuchihara K., and Hashimoto T. Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417 (2002) 193-196
65. Ishida T., and Hashimoto T. An Arabidopsis thaliana tubulin mutant with conditional root-skewing phenotype. J Plant Res 120 (2007) 635-640
66. Abe T., and Hashimoto T. Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43 (2005) 191-204
67. Bannigan A., Wiedemeier A.M., Williamson R.E., Overall R.L., and Baskin T.I. Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47 (2006) 949-958. In rsw6 mutants, cortical arrays have parallel order, but array orientation with respect to the cell axis is randomized. rsw6 may be defective either in a function that links array orientation to the reference frame of the cell or in the ability to maintain array orientation over time
68. Hejnowicz Z. Autonomous changes in the orientation of cortical microtubules underlying the helicoidal cell wall of the sunflower hypocotyl epidermis: spatial variation translated into temporal changes. Protoplasma 225 (2005) 243-256
69. Baskin T.I. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215 (2001) 150-171