Dissecting the molecular mechanism underlying the intimate relationship between cellulose microfibrils and cortical microtubules

Frontiers in Plant Science

Volumn 5, Issue MAR, 2014, Pages

  Lei, Lei ^a   Li, Shundai ^a   Bashline, Logan ^a   Gu, Ying ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Cell expansion; Cell wall; Cellulose synthase complex; CESA interactive proteins; Microtubules

Indexed keywords

EID: 84901003866     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00090     Document Type: Review

References (93)

1. Anderson, C. T., Carroll, A., Akhmetova, L., and Somerville, C. (2010). Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol. 152, 787-796. doi: 10.1104/pp.109.150128
2. Arioli, T., Peng, L., Betzner, A. S., Burn, J., Wittke, W., Herth, W., et al. (1998). Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279, 717-720. doi: 10.1126/science.279.5351.717
3. Baskin, T. I. (2001). On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215, 150-171. doi: 10.1007/BF01280311
4. Beeckman, T., Przemeck, G. K., Stamatiou, G., Lau, R., Terryn, N., De Rycke, R., et al. (2002). Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiol. 130, 1883-1893. doi: 10.1104/pp.102.010603
5. Bischoff, V., Desprez, T., Mouille, G., Vernhettes, S., Gonneau, M., and Hofte, H. (2011). Phytochrome regulation of cellulose synthesis in Arabidopsis. Curr. Biol. 21, 1822-1827. doi: 10.1016/j.cub.2011.09.026
6. Bringmann, M., Li, E., Sampathkumar, A., Kocabek, T., Hauser, M. T., and Persson, S. (2012). POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163-177. doi: 10.1105/tpc.111.093575
7. Burn, J. E., Hocart, C. H., Birch, R. J., Cork, A. C., and Williamson, R. E. (2002). Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiol. 129, 797-807. doi: 10.1104/pp.010931
8. Cano-Delgado, A., Penfield, S., Smith, C., Catley, M., and Bevan, M. (2003). Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J. 34, 351-362. doi: 10.1046/j.1365-313X.2003.01729.x
9. Carpita, N. C. (2011). Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1->4)-beta-D-glycans. Plant Physiol. 155, 171-184. doi: 10.1104/pp.110.163360
10. Carroll, A., Mansoori, N., Li, S., Lei, L., Vernhettes, S., Visser, R. G., et al. (2012). Complexes with mixed primary and secondary cellulose synthases are functional in Arabidopsis plants. Plant Physiol. 160, 726-737. doi: 10.1104/pp.112.199208
11. Chan, J. (2012). Microtubule and cellulose microfibril orientation during plant cell and organ growth. J. Microsc. 247, 23-32. doi: 10.1111/j.1365-2818.2011.03585.x
12. Chan, J., Calder, G., Fox, S., and Lloyd, C. (2007). Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat. Cell Biol. 9, 171-175. doi: 10.1038/ncb1533
13. Chan, J., Crowell, E., Eder, M., Calder, G., Bunnewell, S., Findlay, K., et al. (2010). The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls. J. Cell Sci. 123, 3490-3495. doi: 10.1242/jcs.074641
14. Chen, S., Ehrhardt, D. W., and Somerville, C. R. (2010). Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proc. Natl. Acad. Sci. U.S.A. 107, 17188-17193. doi: 10.1073/pnas.1012348107
15. Crowell, E. F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y. D., Schumacher, K., et al. (2009). Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141-1154. doi: 10.1105/tpc.108.065334
16. Crowell, E. F., Gonneau, M., Stierhof, Y. D., Hofte, H., and Vernhettes, S. (2010). Regulated trafficking of cellulose synthases. Curr. Opin. Plant Biol. 13, 700-705. doi: 10.1016/j.pbi.2010.07.005
17. Davletov, B. A., and Sudhof, T. C. (1993). A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J. Biol. Chem. 268, 26386-26390.
18. Desprez, T., Juraniec, M., Crowell, E. F., Jouy, H., Pochylova, Z., Parcy, F., et al. (2007). Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104, 15572-15577. doi: 10.1073/pnas.0706569104
19. Desprez, T., Vernhettes, S., Fagard, M., Refregier, G., Desnos, T., Aletti, E., et al. (2002). Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol. 128, 482-490. doi: 10.1104/pp.010822
20. Dixit, R., and Cyr, R. (2004a). The cortical microtubule array: from dynamics to organization. Plant Cell 16, 2546-2552. doi: 10.1105/tpc.104.161030
21. Dixit, R., and Cyr, R. (2004b). Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16, 3274-3284. doi: 10.1105/tpc.104.026930
22. Dumais, J., and Forterre, Y. (2012). "Vegetable Dynamicks": the role of water in plant movements. Annu. Rev. Fluid Mech. 44, 453-478. doi: 10.1146/annurev-fluid-120710-101200
23. Edelman, G. M. (1983). Cell adhesion molecules. Science 219, 450-457. doi: 10.1126/science.6823544
24. Endler, A., and Persson, S. (2011). Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4, 199-211. doi: 10.1093/mp/ssq079
25. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., et al. (2000). PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12, 2409-2424. doi: 10.1105/tpc.12.12.2409
26. Fernandes, A. N., Thomas, L. H., Altaner, C. M., Callow, P., Forsyth, V. T., Apperley, D. C., et al. (2011). Nanostructure of cellulose microfibrils in spruce wood. Proc. Natl. Acad. Sci. U.S.A. 108, E1195-E1203. doi: 10.1073/pnas.1108942108
27. Fisher, D. D., and Cyr, R. J. (1998). Extending the Microtubule/Microfibril paradigm. Cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol. 116, 1043-1051. doi: 10.1104/pp.116.3.1043
28. Fujita, M., Himmelspach, R., Hocart, C. H., Williamson, R. E., Mansfield, S. D., and Wasteneys, G. O. (2011). Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis. Plant J. 66, 915-928. doi: 10.1111/j.1365-313X.2011.04552.x
29. Fujita, M., Himmelspach, R., Ward, J., Whittington, A., Hasenbein, N., Liu, C., et al. (2013). The anisotropy1 D604N mutation in the Arabidopsis cellulose synthase1 catalytic domain reduces cell wall crystallinity and the velocity of cellulose synthase complexes. Plant Physiol. 162, 74-85. doi: 10.1104/pp.112.211565
30. Fujita, M., Lechner, B., Barton, D. A., Overall, R. L., and Wasteneys, G. O. (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
31. Gardiner, J. C., Taylor, N. G., and Turner, S. R. (2003). Control of cellulose synthase complex localization in developing xylem. Plant Cell 15, 1740-1748. doi: 10.1105/tpc.012815
32. Giddings, T. H. Jr., Brower, D. L., and Staehelin, L. A. (1980). Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. J. Cell Biol. 84, 327-339. doi: 10.1083/jcb.84.2.327
33. Giddings, T. H., and Staehelin, L. A. (1988). Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium Sp. Planta 173, 22-30. doi: 10.1007/BF00394482
34. Giddings, T. H., and Staehelin, L. A. (1991). "Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis, " in The Cytoskeletal Basis of Plant Growth and Form, ed. C. W. Lloyd (London: Academic Press), 85-99.
35. 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. doi: 10.1007/BF02673872
36. Green, P. B. (1962). Mechanism for plant cellular morphogenesis. Science 138, 1404-1405. doi: 10.1126/science.138.3548.1404
37. Guerriero, G., Fugelstad, J., and Bulone, V. (2010). What do we really know about cellulose biosynthesis in higher plants? J. Integr. Plant Biol. 52, 161-175. doi: 10.1111/j.1744-7909.2010.00935.x
38. Gutierrez, R., Lindeboom, J. J., Paredez, A. R., Emons, A. M. C., and Ehrhardt, D. W. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, 797-806. doi: 10.1038/ncb1886
39. Gu, Y., Kaplinsky, N., Bringmann, M., Cobb, A., Carroll, A., Sampathkumar, A., et al. (2010). Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 107, 12866-12871. doi: 10.1073/pnas.1007092107
40. Gu, Y., and Somerville, C. (2010). Cellulose synthase interacting protein: a new factor in cellulose synthesis. Plant Signal. Behav. 5, 1571-1574. doi: 10.4161/psb.5.12.13621
41. 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. doi: 10.1007/BF01275709
42. Hardham, A. R., and Gunning, B. E. S. (1979). Interpolation of microtubules into cortical arrays during cell elongation and differentiation in roots of Azolla pinnata. J. Cell Sci. 37, 411-442.
43. Heath, I. B. (1974). A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J. Theor. Biol. 48, 445-449. doi: 10.1016/S0022-5193(74)80011-1
44. Hepler, P., and Palevitz, B. A. (1974). Microtubules and microfilaments. Annu. Rev. Plant Physiol. 25, 309-362. doi: 10.1146/annurev.pp.25.060174.001521
45. Herth, W. (1980). Calcofluor white and Congo red inhibit chitin microfibril assembly of Poterioochromonas: evidence for a gap between polymerization and microfibril formation. J. Cell Biol. 87, 442-450. doi: 10.1083/jcb.87.2.442
46. Herth, W. (1983). Arrays of plasma-membrane "rosettes" involved in cellulose microfibril formation of Spirogyra. Planta 159, 347-356. doi: 10.1007/BF00393174
47. 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. doi: 10.1046/j.1365-313X.2003.01906.x
48. Hogetsu, T. (1983). Distribution and local activity of particle complexes synthesizing cellulose microfibrils in the plasma-membrane of Closterium acerosum (Schrank) Ehrenberg. Plant Cell Physiol. 24, 777-781.
49. Holland, N., Holland, D., Helentjaris, T., Dhugga, K. S., Xoconostle-Cazares, B., and Delmer, D. P. (2000). A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol. 123, 1313-1324. doi: 10.1104/pp.123.4.1313
50. Itoh, T. (1976). Microfibrillar orientation of radially enlarged cells of coumarin-and colchicine-treated pine seedlings. Plant Cell Physiol. 17, 385-398.
51. Kimura, S., Laosinchai, W., Itoh, T., Cui, X. J., Linder, C. R., and Brown, R. M. (1999). Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11, 2075-2085.
52. Komis, G., Apostolakos, P., and Galatis, B. (2002). Hyperosmotic stress induces formation of tubulin macrotubules in root-tip cells of Triticum turgidum: their probable involvement in protoplast volume control. Plant Cell Physiol. 43, 911-922. doi: 10.1093/pcp/pcf114
53. Landrein, B., Lathe, R., Bringmann, M., Vouillot, C., Ivakov, A., Boudaoud, A., et al. (2013). Impaired cellulose synthase guidance leads to stem torsion and twists phyllotactic patterns in Arabidopsis. Curr. Biol. 23, 895-900. doi: 10.1016/j.cub.2013.04.013
54. Lane, D. R., Wiedemeier, A., Peng, L., Hofte, H., Vernhettes, S., Desprez, T., et al. (2001). Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-beta-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol. 126, 278-288. doi: 10.1104/pp.126.1.278
55. Ledbetter, M. C., and Porter, K. R. (1963). A "Microtubule" in plant cell fine structure. J. Cell Biol. 19, 239-250. doi: 10.1083/jcb.19.1.239
56. Lei, L., Li, S., Du, J., Bashline, L., and Gu, Y. (2013). CELLULOSE SYNTHASE INTERACTIVE3 regulates cellulose biosynthesis in both a microtubule-dependent and microtubule-independent manner in Arabidopsis. Plant Cell. 25, 4912-4923.
57. Lei, L., Li, S., and Gu, Y. (2012a). Cellulose synthase interactive protein 1 (CSI1) mediates the intimate relationship between cellulose microfibrils and cortical microtubules. Plant Signal. Behav. 7, 714-718. doi: 10.4161/psb.20338
58. Lei, L., Li, S., and Gu, Y. (2012b). Cellulose synthase complexes: composition and regulation. Front. Plant Sci. 3:75. doi: 10.3389/fpls.2012.00075
59. Li, S., Bashline, L., Lei, L., and Gu, Y. (2014). Cellulose synthesis and its regulation. Arabidopsis Book 12:e0169. doi: 10.1199/tab.0169
60. Li, S., Lei, L., and Gu, Y. (2013). Functional analysis of complexes with mixed primary and secondary cellulose synthases. Plant Signal. Behav. 8:e23179. doi: 10.4161/psb.23179
61. Li, S., Lei, L., Somerville, C. R., and Gu, Y. (2011). Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl. Acad. Sci. U.S.A. 109, 185-190. doi: 10.1073/pnas.1118560109
62. Lloyd, C. (2011). Dynamic microtubules and the texture of plant cell walls. Int. Rev. Cell Mol. Biol. 287, 287-329. doi: 10.1016/B978-0-12-386043-9.00007-4
63. Mei, Y., Gao, H. B., Yuan, M., and Xue, H. W. (2012). The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development. Plant Cell 24, 1066-1080. doi: 10.1105/tpc.111.095059
64. Miart, F., Desprez, T., Biot, E., Morin, H., Belcram, K., Hofte, H., et al. (2014). Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis. Plant J. 77, 71-84. doi: 10.1111/tpj.12362
65. Mueller, S. C., and Brown, R. M. Jr. (1980). Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J. Cell Biol. 84, 315-326. doi: 10.1083/jcb.84.2.315
66. Nakamura, M., Ehrhardt, D. W., and Hashimoto, T. (2010). Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12, 1064-1070. doi: 10.1038/ncb2110
67. Nick, P. (2013). Microtubules, signalling and abiotic stress. Plant J. 75, 309-323. doi: 10.1111/tpj.12102
68. Ochoa, W. F., Garcia-Garcia, J., Fita, I., Corbalan-Garcia, S., Verdaguer, N., and Gomez-Fernandez, J. C. (2001). Structure of the C2 domain from novel protein kinase Cepsilon. A membrane binding model for Ca(2+)-independent C2 domains. J. Mol. Biol. 311, 837-849. doi: 10.1006/jmbi.2001.4910
69. Paredez, A. R., Persson, S., Ehrhardt, D. W., and Somerville, C. R. (2008). Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. Plant Physiol. 147, 1723-1734. doi: 10.1104/pp.108.120196
70. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495. doi: 10.1126/science.1126551
71. Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., et al. (2007). Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 15566-15571. doi: 10.1073/pnas.0706592104
72. Richmond, T. (2000). Higher plant cellulose synthases. Genome Biol. 1, reviews3001.1-reviews3001.6. doi: 10.1186/gb-2000-1-4-reviews3001
73. Rickman, C., and Davletov, B. (2003). Mechanism of calcium-independent synaptotagmin binding to target SNAREs. J. Biol. Chem. 278, 5501-5504. doi: 10.1074/jbc.C200692200
74. Roelofsen, P. A., and Houwink, A. L. (1951). Cell wall structure of staminal hairs of Tradescantia virginica and its relation with growth. Protoplasma 40, 1-22. doi: 10.1007/BF01247932
75. Roelofsen, P. A., and Houwink, A. L. (1953). Architecture and growth of the primary cell wall in some plant hairs and in the Phycomyces sporangiophore. Acta Botanica Neerlandica 2, 218-225. doi: 10.1111/j.1438-8677.1953.tb00272.x
76. Sampathkumar, A., Gutierrez, R., McFarlane, H. E., Bringmann, M., Lindeboom, J., Emons, A. M., et al. (2013). Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol. 162, 675-688. doi: 10.1104/pp.113.215277
77. Scheible, W. R., Eshed, R., Richmond, T., Delmer, D., and Somerville, C. (2001). Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc. Natl. Acad. Sci. U.S.A. 98, 10079-10084. doi: 10.1073/pnas.191361598
78. Schrick, K., Debolt, S., and Bulone, V. (2012). Deciphering the molecular functions of sterols in cellulose biosynthesis. Front. Plant Sci. 3:84. doi: 10.3389/fpls.2012.00084
79. Shaw, S. L., Kamyar, R., and Ehrhardt, D. W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718. doi: 10.1126/science.1083529
80. Simons, K., and van Meer, G. (1988). Lipid sorting in epithelial cells. Biochemistry 27, 6197-6202. doi: 10.1021/bi00417a001
81. Skotheim, J. M., and Mahadevan, L. (2005). Physical limits and design principles for plant and fungal movements. Science 308, 1308-1310. doi: 10.1126/science.1107976
82. Somerville, C. (2006). Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Biol. 22, 53-78. doi: 10.1146/annurev.cellbio.22.022206.160206
83. Sugimoto, K., Williamson, R. E., and Wasteneys, G. O. (2000). New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol. 124, 1493-1506. doi: 10.1104/pp.124.4.1493
84. Taylor, N. G., Howells, R. M., Huttly, A. K., Vickers, K., and Turner, S. R. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. U.S.A. 100, 1450-1455. doi: 10.1073/pnas.0337628100
85. Taylor, N. G., Laurie, S., and Turner, S. R. (2000). Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12, 2529-2540. doi: 10.1105/tpc.12.12.2529
86. Thomas, L. H., Forsyth, V. T., Sturcova, A., Kennedy, C. J., May, R. P., Altaner, C. M., et al. (2013). Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol. 161, 465-476. doi: 10.1104/pp.112.206359
87. van Meer, G., and Simons, K. (1988). Lipid polarity and sorting in epithelial cells. J. Cell. Biochem. 36, 51-58. doi: 10.1002/jcb.240360106
88. Vaughn, K. C., and Harper, J. D. (1998). Microtubule-organizing centers and nucleating sites in land plants. Int. Rev. Cytol. 181, 75-149. doi: 10.1016/S0074-7696(08)60417-9
89. 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. doi: 10.1111/j.1365-313X.2008.03444.x
90. Wyatt, S. E., and Carpita, N. C. (1993). The plant cytoskeleton-cell-wall continuum. Trends. Cell Biol. 3, 413-417. doi: 10.1016/0962-8924(93)90022-S
91. Zhang, T., Mahgsoudy-Louyeh, S., Tittmann, B., and Cosgrove, D. J. (2013). Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis. Cellulose doi: 10.1007/s10570-013-9996-1
92. Zhong, R., Burk, D. H., Morrison, W. H. III, 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. doi: 10.1105/tpc.005801
93. Zhu, C., and Dixit, R. (2011). Single molecule analysis of the Arabidopsis FRA1 kinesin shows that it is a functional motor protein with unusually high processivity. Mol. Plant 4, 879-885. doi: 10.1093/mp/ssr077