Pausing of golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis

Plant Cell

Volumn 21, Issue 4, 2009, Pages 1141-1154

  Crowell, Elizabeth Faris ^a   Bischoff, Volker ^a   Desprez, Thierry ^a   Rolland, Aurélia ^a   Stierhof, York Dieter ^b   Schumacher, Karin ^c   Gonneau, Martine ^a   Höfte, Herman ^a   Vernhettes, Samantha ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 66149192394     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.065334     Document Type: Article

References (58)

1. Baskin, T.I. (2001). On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma 215: 150-171.
2. Baskin, T.I. (2005). Anisotropic expansion of the plant cell wall. Annu. Rev. Cell Dev. Biol. 21: 203-222.
3. Bowling, A.J., and Brown, R.M., Jr. (2008). The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. Protoplasma 233: 115-127.
4. Chan, J., Calder, G.M., Doonan, J.H., and Lloyd, C.W. (2003). EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat. Cell Biol. 5: 967-971.
5. Chan, J., Calder, G.M., Fox, S., and Lloyd, C.W. (2007). Cortical microtubule arrays undergo rotary movements in Arabidopsis hypo-cotyl epidermal cells. Nat. Cell Biol. 9: 171-175.
6. Chuong, S.D., Park, N.I., Freeman, M.C., Mullen, R.T., and Muench, D.G. (2005). The peroxisomal multifunctional protein interacts with cortical microtubules in plant cells. BMC Cell Biol. 6: 40.
7. daSilva, L.L., Snapp, E.L., Denecke, J., Lippincott-Schwartz, J., Hawes, C, and Brandizzi, F. (2004). Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16: 1753-1771.
8. DeBol.t, S., Gutierrez, R., Ehrhardt, D.W., Melo, C.V., Ross, L., Cutler, S.R., Somerville, C, and Bonetta, D. (2007a). Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proc. Natl. Acad. Sci. USA 104: 5854-5859.
9. DeBol.t, S., Gutierrez, R., Ehrhardt, D.W., and Somerville, C. (2007b). Nonmotile cellulose synthase subunits repeatedly accumulate within localized regions at the plasma membrane in arabidopsis hypocotyl cells following 2,6-dichlorobenzonitrile treatment. Plant Physiol. 145: 334-338.
10. Desprez, T., Juraniec, M., Crowell, E.F., Jouy, H., Pochylova, Z., Parcy, F., Höfte, H., Gonneau, M., and Vernhettes, S. (2007). Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 15572-15577.
11. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
12. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., and Friml, J. (2007). Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17: 520-527.
13. Emons, A.M.C. (1982). Microtubules do not control microfibril orientation in a helicoidal wall. Protoplasma 113: 85-87.
14. Estelle, M.A., and Somerville, C.R. (1987). Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206: 200-206.
15. Foissner, I., and Wasteneys, G.O. (2007). Wide-ranging effects of eight cytochalasins and latrunculin A and B on intracellular motility and actin filament reorganization in characean internodal cells. Plant Cell Physiol. 48: 585-597.
16. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M., and Höfte, H. (1997). Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114: 295-305.
17. Granger, C.L., and Cyr, R.J. (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: 201-214.
18. Green, P.B. (1962). Mechanism for plant cellular morphogenesis. Science 138: 1404-1405.
19. Green, P.B., and Selker, J.M.L. (1991). Mutual alignments of cell walls, cellulose and cytoskeletons: Their role in meristems. In The Cytoskel-etal Basis of Plant Growth and Form, C.W. Lloyd, ed (London: Academic Press), pp. 303-322.
20. Haigler, C.H., and Brown, R.M. (1986). Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma 134: 111-120.
21. Hepler, P.K., and Newcomb, E.H. (1964). Microtubules and fibrils in the cytoplasm of Coleus cells undergoing secondary wall deposition. J. Cell Biol. 20: 529-532.
22. Herth, W. (1985). Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164: 12-21.
23. Himmelspach, R., Williamson, R.E., and Wasteneys, G.O. (2003). Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J. 36: 565-575.
24. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
25. Kimura, S., Laosinchai, W., Itoh, T., Cui, X., under, C.R., and Brown, R.M., Jr. (1999). Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant vigna angularis. Plant Cell 11:2075-2086.
26. Ledbetter, M.C., and Porter, K.R. (1963). A " microtubule" in plant cell fine structure. J. Cell Biol. 19: 239-250.
27. Lu, L., Lee, Y.R., Pan, R., Maloof, J.N., and 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.
28. Marc, J., Granger, C.L., Brincat, J., Fisher, D.D., Kao, Th., McCubbin, A.G., and Cyr, R.J. (1998). A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10: 1927-1940.
29. Marion, J., Bach, L., Bellec, Y., Meyer, C, Gissot, L., and Faure, J.D. (2008). Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J. 56: 169-179.
30. McFarlane, H.E., Young, R.E., Wasteneys, G.O., and Samuels, A.L. (2008). Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells. Planta 227: 1363-1375.
31. Mouille, G., Robin, S., Lecomte, M., Pagant, S., and Höfte, H. (2003). Classification and identification of Arabidopsis cell wall mutants using Fourier-transform infrared (FT-IR) microspectroscopy. Plant J. 35: 393-404.
32. Mueller, S.C., and Brown, R.M., Jr. (1980). Evidence for an intra-membrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J. Cell Biol. 84: 315-326.
33. Nebenführ, A., Gallagher, L.A., Dunahay, T.G., Frohlick, J.A., Mazurkiewicz, A.M., Meehl, J.B., and Staehelin, L.A. (1999). Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121: 1127-1142.
34. Paredez, A.R., Somerville, C.R., and Ehrhardt, D.W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491-1495.
35. Peng, L., Xiang, F., Roberts, E., Kawagoe, Y., Greve, L.C., Kreuz, K., and Delmer, D.P. (2001). The experimental herbicide CGA 325'615 inhibits synthesis of crystalline cellulose and causes accumulation of non-crystalline beta-1,4-glucan associated with CesA protein. Plant Physiol. 126: 981-992.
36. Probine, M.C., and Preston, R.D. (1961). Cell growth and the structure and mechanical properties of the wall in internodal cells of Nitella opaca. I. Wall structure and growth. J. Exp. Bot. 12: 261-282.
37. Probine, M.C., and Preston, R.D. (1962). Cell growth and the structure and mechanical properties of the wall in internodal cells of Nitella opaca. II. Mechanical properties of the walls. J. Exp. Bot. 13: 111-127.
38. Refregier, G., Pelletier, S., Jaillard, D., and Höfte, H. (2004). Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol. 135: 959-968.
39. Reichardt, I., Stierhof, Y.D., Mayer, U., Richter, S., Schwarz, H., Schumacher, K., and Jurgens, G. (2007). Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17:2047-2053.
40. Reiter, W.D., Chappie, C.C., and Somerville, C.R. (1993). Altered growth and cell walls in a fucose-deficient mutant of arabidopsis. Science 261: 1032-1035.
41. Ripper, D., Schwarz, H., and Stierhof, Y.D. (2008). Cryo-section immunolabelling of difficult to preserve specimens: advantages of cryofixation, freeze-substitution and rehydration. Biol. Cell 100: 109-123.
42. Robert, S., Chary, S.N., Drakakaki, G., Li, S., Yang, Z., Raikhel, N.V., and Hicks, G.R. (2008). Endosidinl defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc. Natl. Acad. Sci. USA 105: 8464-8469.
43. Robin, S., Lecomte, M., Höfte, H., and Mouille, G. (2003). A procedure for the clustering of cell wall mutants in the model plant Arabidopsis based on fourier-transform infrared (FT-IR) spectroscopy. J. Appl. Stat. 30: 669-681.
44. Robinson, D.G., Jiang, L., and Schumacher, K. (2008). The endo-somal system of plants: Charting new and familiar territories. Plant Physiol. 147: 1482-1492.
45. Rudolph, U. (1987). Occurrence of rosettes in the ER membrane of young Funaría hygrometríca protonemata. Naturwissenschaften 74: 439.
46. Sainsbury, F., Collings, D.A., Mackun, K., Gardiner, J., Harper, J.D.I., and Marc, J. (2008). Developmental reorientation of transverse cortical microtubules to longitudinal directions: A role for actomyosin-based streaming and partial microtubule-membrane detachment. Plant J. 56: 116-131.
47. Scott, T.A., and Melvin, E.H. (1953). Determination of dextran with anthrone. Anal. Biochem. 25: 1656-1661.
48. Shaw, S.L., Kamyar, R., and Ehrhardt, D.W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300: 1715- 1718.
49. Smith, L.G., and Oppenheimer, D.G. (2005). Spatial control of cell expansion by the plant cytoskeleton. Annu. Rev. Cell Dev. Biol. 21: 271-295.
50. Somerville, C. (2006). Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Biol. 22: 53-78.
51. Sparkes, I.A., Teanby, N.A., and Hawes, C. (2008). Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: A genetic tool for the next generation. J. Exp. Bot. 59:2499-2512.
52. Sugimoto, K., Himmelspach, R., Williamson, R.E., and Wasteneys, G.O. (2003). Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15: 1414-1429.
53. Ueda, K., Matsuyama, T., and Hashimoto, T. (1999). Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Proto-plasma206: 201-206.
54. Updegraff, D.M. (1969). Semi-micro determination of cellulose in biological materials. Anal. Biochem. 32: A20-A2A.
55. Voigt, B., Timmers, A.C., Samaj, J., Muller, J., Baluska, F., and Menzel, D. (2005). GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur. J. Cell Biol. 84: 595-608.
56. Westermann, S., Wang, H.W., Avila-Sakar, A., Drubin, D.G., Nogales, E., and Barnes, G. (2006). The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440: 565-569.
57. Wightman, R., and Turner, S.R. (2008). The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J. 54: 794-805.
58. Zhong, R., Burk, D.H., Morrison III, W.H., and Ye, Z.H. (2002). A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14: 3101-3117.