Microtubule cortical array organization and plant cell morphogenesis

Current Opinion in Plant Biology

Volumn 9, Issue 6, 2006, Pages 571-578

  Paradez, Alex ^a,b   Wright, Amanda ^c   Ehrhardt, David W ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL GROWTH; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROTUBULE; PLANT; REVIEW;

CELL GROWTH PROCESSES; MICROTUBULES; PLANTS;

EID: 33749555581     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2006.09.005     Document Type: Review

References (59)

1. Lloyd C., and Seagull R.W. A new spring for plant cell biology: microtubules as dynamic helices. Trends Biochem Sci 10 (1985) 476-478
2. Fu Y., Gu Y., Zheng Z., Wasteneys G., and Yang Z. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120 (2005) 687-700. Evidence for a mechanism that exerts local control over cytoskeletal organization in plant cells. Evidence is presented that the small G-protein ROP2 and a ROP2-interacting protein, RIC1, regulate microtubule organization and cell lobing in pavement cells. A model is suggested by which ROP2 negatively regulates RIC1 in cell lobes, and RIC1 actively promotes microtubule assembly or stabilization in cell sinuses.
3. Green P.B. Mechanism for plant cell morphogenesis. Science 138 (1962) 1404
4. Ledbetter M.C., and Porter K.R. A 'microtubule' in plant cell fine structure. J Cell Biol 19 (1963) 239-250
5. Lloyd C.W., Clayton L., Dawson P.J., Doonan J.H., Hulme J.S., Roberts I.N., and Wells B. The cytoskeleton underlying side walls and cross walls in plants: molecules and macromolecular assemblies. J Cell Sci Suppl 2 (1985) 143-155
6. Palevitz B: Potential significance of microtubule rearrangement, translocation and reutilization in plant cells. In The Cytoskeletal Basis of Plant Growth and Form. Edited by Lloyd C. Academic Press; 1991:45-55.
7. Baskin T.I. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215 (2001) 150-171
8. Sugimoto K., Williamson R.E., and Wasteneys G.O. New techniques enable comparative analysis of microtubule orientation; wall texture; and growth rate in intact roots of Arabidopsis. Plant Physiol 124 (2000) 1493-1506
9. Sugimoto K., Himmelspach R., Williamson R.E., and Wasteneys G.O. Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15 (2003) 1414-1429
10. Cyr R. Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol 10 (1994) 153-180
11. Cyr R.J., and Palevitz B.A. Organization of cortical microtubules in plant cells. Curr Opin Cell Biol 7 (1995) 65-71
12. Lambert A. Microtubule-organizing centers in higher plants: evolving concepts. Bot Acta 108 (1995) 535-537
13. Liu B., Joshi H.C., Wilson T.J., Silflow C.D., Palevitz B.A., and Snustad D.P. γ-Tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6 (1994) 303-314
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 γ-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115 (2002) 2423-2431
15. Seltzer V., Pawlowski T., Campagne S., Canaday J., Erhardt M., Evrard J.L., Herzog E., and Schmit A.C. Multiple microtubule nucleation sites in higher plants. Cell Biol Int 27 (2003) 267-269
16. 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. Genetic analysis demonstrates that γ-tubulin function is crucial for microtubule organization throughout the cell cycle.
17. Shaw S., Kamyar R., and Ehrhardt D. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300 (2003) 1715-1718
18. Chan J., Calder G., Doonan J., and Lloyd C. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5 (2003) 967-971
19. 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 γ-tubulin in higher plants. Nat Cell Biol 7 (2005) 961-968. In vitro and in vivo assays demonstrate γ-tubulin-dependent microtubule nucleation from the walls of existing microtubules. New polymers grow within a narrow range of angles, around 40°, relative to the existing microtubule.
20. Van Damme D., Van Poucke K., Boutant E., Ritzenthaler C., Inzé D., and Geelen D. In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136 (2004) 3956-3967
21. Wasteneys G., and Williamson R. Microtubule resassembly in internodal cell of Nitella tasmanica: assembly of cortical microtubules in branching clusters and its relevance to steady state microtubule assembly. J Cell Sci 93 (1989) 705-714
22. Wasteneys G., Gunning B., and Hepler P. Microinjection of fluorescent brain tubulin reveals dynamic properties of cortical microtubules in living plant cells. Cell Motil Cytoskel 24 (1993) 205-213
23. Yuan M., Shaw P., Warn R., and Lloyd C. Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc Natl Acad Sci USA 91 (1994) 6050-6053
24. Wymer C.L., Fisher D.D., Moore R.C., and Cyr R.J. Elucidating the mechanism of cortical microtubule reorientation in plant cells. Cell Motil Cytoskeleton 35 (1996) 162-173
25. Ehrhardt D.W., and Shaw S.L. Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57 (2006) 859-875
26. Dhonukshe P., and Gadella Jr. T.W. Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15 (2003) 597-611
27. Vos J., Dogterom M., and Emons A. Microtubules become more dynamic but not shorter during preprophase band formation: a possible 'search-and-capture' mechanism for microtubule translocation. Cell Motil Cytoskeleton 57 (2004) 246-258
28. Gardiner J., Harper J., Weerakoon N., Collings D., Ritchie S., Gilroy S., Cyr R., and Marc J. A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13 (2001) 2143-2158
29. 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
30. 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
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. Mathur J., Mathur N., Kernebeck B., Srinivas B.P., and Hülskamp M. A novel localization pattern for an EB1-like protein links microtubules dynamics to endomembrane organization. Curr Biol 13 (2003) 1991-1997
33. 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 USA 96 (1999) 14931-14936
34. 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
35. 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
36. 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
37. 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. FRAP experiments show that MAP65-1 protein on microtubule bundles turns over much faster than microtubule treadmilling. This is an important property for a cross-linking protein that is found in bundles composed of highly dynamic constituent polymers.
38. Smertenko A.P., Chang H.Y., Sonobe S., Fenyk S.I., Weingartner M., Bögre 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 localization and function in the mitotic spindle is shown to be regulated by CDK- and MAPK-dependent phosphorylation.
39. 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. Analysis of microtubule orientation in hundreds of sunflower hypocotyl cells, together with mathematical modeling, suggests that the observed distributions of array orientations are consistent with a model in which array orientation in these cells is constantly rotating or oscillating.
40. 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. Mutations in the SPR1 gene family are shown to be additive, resulting in pronounced loss of cell expansion anisotropy.
41. 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
42. 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
43. Abe T., Thitamadee S., and Hashimoto T. Microtubule defects and cell morphogenesis in the lefty1 lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol 45 (2004) 211-220
44. Abe T., and Hashimoto T. Altered microtubule dynamics by expression of modified α-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43 (2005) 191-204. Modifications of the C-terminus of α-tubulin act dominantly to reduce microtubule dynamicity and cause right-handed twisting of organ growth. The authors present evidence that these alterations might reduce the rate of GTP hydrolysis, stabilizing and extending the G-cap on microtubule plus ends.
45. 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 the rsw-6 mutant, microtubule arrays in root cells are randomized with respect to axial orientation, but retain parallel architecture. rsw6 might be defective in a function that links microtubule orientation within the cellular reference frame, or in coordinating the orientation of arrays across neighboring cells.
46. Somerville C: Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 2006, in press.
47. Paredez A.R., Somerville C.R., and Ehrhardt D.W. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312 (2006) 1491-1495. Spinning disk confocal microscopy of a functional YFP{proportion}CESA6 fusion protein allows the observation of dynamic cellulose synthase complexes in the plant cell membrane for the first time. Membrane protein complexes that contain CESA6 are shown to track the positions of cortical microtubules and to re-organize their positions and trajectories as microtubules are reorganized.
48. Heath I.B. A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48 (1974) 445-449
49. Mulder B., Schel J., and Emons A.M. How the geometrical model for plant cell wall formation enables the production of a random texture. Cellulose 11 (2004) 395-401
50. Taylor N.G., Howells R.M., Huttly A.K., Vickers K., and Turner S.R. Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100 (2003) 1450-1455
51. Sonobe S., Yamamoto S., Motomura M., and Shimmen T. Isolation of cortical MTs from tobacco BY-2 cells. Plant Cell Physiol 42 (2001) 162-169
52. Lee Y.R., and Liu B. Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136 (2004) 3877-3883
53. 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. Imaging of EB1 in tobacco tissue culture cells and in transformed Arabidopsis reveals that many cells display regional and global patterns of preferred co-orientation of cortical microtubules with respect to polymer polarity.
54. Giddings T.H., and Staehelin L.A. Spatial relationship between micotubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp. Planta 173 (1988) 22-30
55. Wasteneys G.O., and Fujita M. Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J Plant Res 119 (2006) 5-10
56. Robert S., Bichet A., Grandjean O., Kierzkowski D., Satiat-Jeunemaitre B., Pelletier S., Hauser M.T., Höfte H., and Vernhettes S. An Arabidopsis endo-1,4-beta-d-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17 (2005) 3378-3389. KORRIGAN protein is shown to localize to a variety of intracellular compartments including Golgi, an early endosomal compartment, the tonoplast, and a fourth compartment that is distinct from the others. This fourth compartment appears to be localized at the cell cortex and accumulates in response to treatment with the cellulose synthase inhibitor isoxoben. The compartment exhibits microtubule-dependent motility. It is proposed that KORRIGAN activity might be regulated by intracellular recycling.
57. Persson S., Wei H., Milne J., Page G.P., and Somerville C.R. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102 (2005) 8633-8638
58. Muench D.G., Chuong S.D., Franceschi V.R., and Okita T.W. Developing prolamine protein bodies are associated with the cortical cytoskeleton in rice endosperm cells. Planta 211 (2000) 227-238
59. Persson S., Wei H., Milne J., Page G.P., and Somerville C.R. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102 (2005) 8633-8638