biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:363-377, 2020 | DOI: 10.32615/bp.2020.065

Cellulose biosynthesis in plants - the concerted action of CESA and non-CESA proteins

M. JURANIEC*, B. GAJDA
Department of Plant Ecophysiology, Faculty of Biology and Environmental Protection, University of Lodz, PL-90237 Lodz, Poland

Cellulose is the most abundant polysaccharide produced by plants. In the form of rigid microfibrils surrounding the cells, cellulose constitutes the load-bearing cell wall element that controls cell growth and shape. Cellulose microfibrils are laid down outside the cell by the multimeric plasma membrane-inserted cellulose synthase complexes (CSCs), which move along underlying cortical microtubules (CMTs). In plants, CSCs are shaped as rosettes with six lobes symmetrically arranged in a hexagonal structure. In Arabidopsis, the CSC is composed of at least three functionally non-redundant cellulose synthase (CESA) glycosyltransferases in both primary and secondary cell walls. The number, organization, and interactions of CESA proteins within the CSC have been debated for many years on the basis of numerous lines of evidence provided by electron microscopy, biochemical and genetic approaches, spectroscopic techniques, as well as computational modeling. The Arabidopsis thaliana model was extremely useful in elucidating the molecular composition of CSC and enabled to elucidate the specialized functions of distinct AtCESA isoforms. Several additional, non-CESA proteins involved in cellulose synthesis and its regulation were also identified in Arabidopsis. This review outlines the latest findings on CSC organization, trafficking, and plant-specific proteins directly associated with the complex and interconnecting CESAs with CMTs.

Keywords: Arabidopsis thaliana, cellulose microfibrils, cellulose synthase complex, cortical microtubules, membrane proteins, mutants.

Received: July 17, 2019; Revised: October 25, 2019; Accepted: January 2, 2020; Prepublished online: May 13, 2020; Published online: May 14, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
JURANIEC, M., & GAJDA, B. (2020). Cellulose biosynthesis in plants - the concerted action of CESA and non-CESA proteins. Biologia plantarum, 64, Article 363-377. https://doi.org/10.32615/bp.2020.065
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Amor, Y., Haigler, C.H., Johnson, S., Wainscott, M., Delmer, D.P.: A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. - Proc. nat. Acad. Sci. USA 92: 9353-9357, 1995. Go to original source...
    2. Appenzeller, L., Doblin, M., Barreiro, R., Wang, H., Niu, X., Kollipara, K., Carrigan, L., Tomes, D., Chapman, M., Dhugga, K.S.: Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. - Cellulose 11: 287-299, 2004. Go to original source...
    3. Arioli, T., Peng, L., Betzner, A.S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Höfte, H., Plazinski, J., Birch, R., Cork, A., Glover, J., Redmond, J., Williamson, R.E.: Molecular analysis of cellulose biosynthesis in Arabidopsis. - Science 279: 717-720, 1998. Go to original source...
    4. Atanassov, I.I., Pittman, J.K., Turner, S.R.: Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Arabidopsis secondary cell walls. - J. biol. Chem. 284: 3833-3841, 2009. Go to original source...
    5. Bashline, L., Li, S., Anderson, C.T., Lei, L., Gu, Y.: The endocytosis of cellulose synthase in Arabidopsis is dependent on μ2, a clathrin-mediated endocytosis adaptin. - Plant Physiol. 163: 150-160, 2013. Go to original source...
    6. Bashline, L., Li, S., Zhu, X., Gu, Y.: The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. - Proc. nat. Acad. Sci. USA 112: 12870-12875, 2015. Go to original source...
    7. Benfey, P.N., Linstead, P.J., Roberts, K., Schiefelbein, J.W., Hauser, M.T., Aeschbacher, R.A.: Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. - Development 119: 57-70, 1993. Go to original source...
    8. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., Benfey, P.N.: A gene expression map of the Arabidopsis root. - Science 302: 1956-1960, 2003. Go to original source...
    9. Bischoff, V., Desprez, T., Mouille, G., Vernhettes, S., Gonneau, M., Höfte, H.: Phytochrome regulation of cellulose synthesis in Arabidopsis. - Curr. Biol. 21: 1822-1827, 2011. Go to original source...
    10. Bowling, A.J., Brown, R.M., Jr.: The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. - Protoplasma 233: 115-127, 2008. Go to original source...
    11. Bringmann, M., Li, E., Sampathkumar, A., Kocabek, T., Hauser, M.T., Persson, S.: POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. - Plant Cell 24: 163-177, 2012. Go to original source...
    12. Brown, D.M., Zeef, L.A.H., Ellis, J., Goodacre, R., Turner, S.R.: Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. - Plant Cell 17: 2281-2295, 2005. Go to original source...
    13. Burton, R.A., Shirley, N.J., King, B.J., Harvey, A.J., Fincher, G.B.: The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. - Plant Physiol. 134: 224-236, 2004. Go to original source...
    14. Caño-Delgado, A., Penfield, S., Smith, C., Catley, M., Bevan, M.: Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. - Plant J. 34: 351-362, 2003. Go to original source...
    15. Carroll, A., Mansoori, N., Li, S., Lei, L., Vernhettes, S., Visser, R.G., Somerville, C., Gu, Y., Trindade, L.M.: Complexes with mixed primary and secondary cellulose synthases are functional in Arabidopsis plants. - Plant Physiol. 160: 726-737, 2012. Go to original source...
    16. Carroll, A., Specht, C.D.: Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences. - Front. Plant Sci. 2: 5, 2011. Go to original source...
    17. Chan, J., Calder, G., Fox, S., Lloyd, C.: Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. - Nat. cell. Biol. 9: 171-175, 2007. Go to original source...
    18. Chan, J., Crowell, E., Eder, M., Calder, G., Bunnewell, S., Findlay, K., Vernhettes, S., Höfte, H., Lloyd, C.: 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, 2010. Go to original source...
    19. Chanzy, H., Imada, K., Mollard, A., Vuong, R., Barnoud, F.: Crystallographic aspects of sub-elementary cellulose fibrils occurring in the wall of rose cells cultured in vitro. - Protoplasma 100: 303-316, 1979. Go to original source...
    20. Chanzy, H., Imada, K., Vuong, R.: Electron diffraction from the primary wall of cotton fibers. - Protoplasma 94: 299-306, 1978. Go to original source...
    21. Chen, S., Ehrhardt, D.W., Somerville, C.R.: Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. - Proc. nat. Acad. Sci. USA 107: 17188-17193, 2010. Go to original source...
    22. Chen, X., Wu, S., Liu, Z., Friml, J.: Environmental and endogenous control of cortical microtubule orientation. - Trends cell. Biol. 26: 409-419, 2016. Go to original source...
    23. Cifuentes, C., Bulone, V., Emons, A.M.: Biosynthesis of callose and cellulose by detergent extracts of tobacco cell membranes and quantification of the polymers synthesized in vitro. - J. integr. Plant Biol. 52: 221-233, 2010. Go to original source...
    24. Crowell, E.F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y.D., Schumacher, K., Gonneau, M., Höfte, H., Vernhettes, S.: Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. - Plant Cell 21: 1141-1154, 2009. Go to original source...
    25. Delmer, D.P.: Cellulose biosynthesis: exciting times for a difficult field of study. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 245-276, 1999. Go to original source...
    26. Desprez, T., Juraniec, M., Crowell, E.F., Jouy, H., Pochylova, Z., Parcy, F., Höfte, H., Gonneau, M., Vernhettes, S.: Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 104: 15572-15577, 2007. Go to original source...
    27. Ding, S.Y., Himmel, M.E.: The maize primary cell wall microfibril: a new model derived from direct visualization. - J. Agr. Food Chem. 54: 597-606, 2006. Go to original source...
    28. Djerbi, S., Lindskog, M., Arvestad, L., Sterky, F., Teeri, T.T.: The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. - Planta 221: 739-746, 2005. Go to original source...
    29. Doblin, M.S., Kurek, I., Jacob-Wilk, D., Delmer, D.P.: Cellulose biosynthesis in plants: from genes to rosettes. - Plant Cell Physiol. 43: 1407-1420, 2002. Go to original source...
    30. Donaldson, L.: Cellulose microfibril aggregates and their size variation with cell wall type. - Wood Sci. Technol. 41: 443-460, 2007. Go to original source...
    31. Endler, A., Kesten, C., Schneider, R., Zhang, Y., Ivakov, A., Froehlich, A., Funke, N., Persson, S.: A mechanism for sustained cellulose synthesis during salt stress. - Cell 162: 1353-1364, 2015. Go to original source...
    32. Eskandari, S., Wright, E.M., Kreman, M., Starace, D.M., Zampighi, G.A.: Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy. - Proc. nat. Acad. Sci. USA 95: 11235-11240, 1998. Go to original source...
    33. Facette, M.R., Shen, Z., Björnsdóttir, F.R., Briggs, S.P., Smith, L.G.: Parallel proteomic and phosphoproteomic analyses of successive stages of maize leaf development. - Plant Cell 25: 2798-2812, 2013. Go to original source...
    34. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S., Höfte, H.: PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. - Plant Cell 12: 2409-2424, 2000. Go to original source...
    35. Fernandes, A.N., Thomas, L.H., Altaner, C.M., Callow, P., Forsyth, V.T., Apperley, D.C., Kennedy, C.J., Jarvis, M.C.: Nanostructure of cellulose microfibrils in spruce wood. - Proc. nat. Acad. Sci. USA 108: E1195-E1203, 2011. Go to original source...
    36. Gardiner, J.C., Taylor, N.G., Turner, S.R.: Control of cellulose synthase complex localization in developing xylem. - Plant Cell 15: 1740-1748, 2003. Go to original source...
    37. Gonneau, M., Desprez, T., Guillot, A., Vernhettes, S., Höfte, H.: Catalytic subunit stoichiometry within the cellulose synthase complex. - Plant Physiol. 166: 1709-1712, 2014. Go to original source...
    38. Gu, Y., Kaplinsky, N., Bringmann, M., Cobb, A., Carroll, A., Sampathkumar, A., Baskin, T.I., Persson, S., Somerville, C.R.: Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. - Proc. nat. Acad. Sci. USA 107: 12866-12871, 2010. Go to original source...
    39. Gutierrez, R., Lindeboom, J.J., Paredez, A.R., Emons, A.M., Ehrhardt, D.W.: Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. - Nat. Cell Biol. 11: 797-806, 2009. Go to original source...
    40. Ha, M.A., Apperley, D.C., Evans, B.W., Huxham, I.M., Jardine, W.G., Viëtor, R.J., Reis, D., Vian, B., Jarvis, M.C.: Fine structure in cellulose microfibrils: NMR evidence from onion and quince. - Plant J. 16: 183-190, 1998. Go to original source...
    41. Haigler, C.H., Brown, R.M.: 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, 1986. Go to original source...
    42. Hauser, M.T., Morikami, A., Benfey P.N.: Conditional root expansion mutants of Arabidopsis. - Development 121: 1237-1252, 1995. Go to original source...
    43. Herth, W.: Arrays of plasma-membrane 'rosettes' involved in cellulose microfibril formation of Spirogyra. - Planta 159: 347-356, 1983. Go to original source...
    44. Hill, J.L., Jr., Hammudi, M.B., Tien, M.: The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. - Plant Cell 26: 4834-4842, 2014. Go to original source...
    45. Hill, J.L., Jr., Hill, A.N., Roberts, A.W., Haigler, C.H., Tien, M.: Domain swaps of Arabidopsis secondary wall cellulose synthases to elucidate their class specificity. - Plant Direct 2: e00061, 2018. Go to original source...
    46. Kennedy, C.J., Cameron, G.J., ©turcová, A., Apperley, D.C., Altaner, C., Wess, T.J., Jarvis, M.C.: Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence. - Cellulose 14: 235-246, 2007. Go to original source...
    47. Kerstens, S., Verbelen, J.P.: Cellulose orientation at the surface of the Arabidopsis seedling. Implications for the biomechanics in plant development. - J. Struct. Biol. 144: 262-270, 2003. Go to original source...
    48. Kesten, C., Menna, A., Sánchez-Rodríguez, C.: Regulation of cellulose synthesis in response to stress. - Curr. Opin. Plant Biol. 40: 106-113, 2017. Go to original source...
    49. Kim, W.C., Ko, J.H., Han, K.H.: Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. - Plant mol. Biol. 78: 489-501, 2012. Go to original source...
    50. Kim, W.C., Ko, J.H., Kim, J.Y., Kim, J., Bae, H.J., Han, K.H.: MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. - Plant J. 73: 26-36, 2013. Go to original source...
    51. Kimura, S., Laosinchai, W., Itoh, T., Cui, X., Linder, C.R., Brown, R.M.: Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. - Plant Cell 11: 2075-2086, 1999. Go to original source...
    52. Ko, J.H., Kim, W.C., Han, K.H.: Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. - Plant J. 60: 649-665, 2009. Go to original source...
    53. Kudlicka, K., Brown, R.M. Jr.: Cellulose and callose biosynthesis in higher plants. I. solubilization and separation of (1→3)- and (1→4)-β-glucan synthase activities from mung bean. - Plant Physiol. 115: 643-656, 1997. Go to original source...
    54. Kurek, I., Kawagoe, Y., Jacob-Wilk, D., Doblin, M., Delmer D.: Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. - Proc. nat. Acad. Sci. USA 99: 11109-11114, 2002. Go to original source...
    55. Lai-Kee-Him, J., Chanzy, H., Müller, M., Putaux, J.L., Imai, T., Bulone, V.: In vitro versus in vivo cellulose microfibrils from plant primary wall synthases: structural differences. - J. biol. Chem. 277: 36931-36939, 2002. Go to original source...
    56. Lane, D.R., Wiedemeier, A., Peng, L., Höfte, H., Vernhettes, S., Desprez, T., Hocart, C.H., Birch, R.J., Baskin, T.I., Burn, J.E., Arioli, T., Betzner, A.S., Williamson, R.E.: Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. - Plant Physiol. 126: 278-288, 2001. Go to original source...
    57. Lei, L., Li, S., Gu, Y.: Cellulose synthase interactive protein 1 (CSI1) mediates the intimate relationship between cellulose microfibrils and cortical microtubules. - Plant Signal. Behav. 7: 1-5, 2012. Go to original source...
    58. Lei, L., Singh, A., Bashline, L., Shundai, Li., Yingling, Y.G., Gu, Y.: CELLULOSE SYNTHASE INTERACTIVE1 is required for fast recycling of cellulose synthase complexes to the plasma membrane in Arabidopsis. - Plant Cell 27: 2926-2940, 2015. Go to original source...
    59. Lertpiriyapong, K., Sung, Z.R.: The elongation defective1 mutant of Arabidopsis is impaired in the gene encoding a serine-rich protein. - Plant mol. Biol. 53: 581-595, 2003. Go to original source...
    60. Li, S., Lei, L., Gu, Y.: Functional analysis of complexes with mixed primary and secondary cellulose synthases. - Plant Signal. Behav. 8: e23179, 2013. Go to original source...
    61. Li, S., Lei, L., Somerville, C.R., Gu, Y.: Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. - Proc. nat. Acad. Sci. USA 109: 185-190, 2012. Go to original source...
    62. Lin, F.C., Brown, R.M., Jr., Drake, R.R., Jr., Haley, B.E.: Identification of the uridine 5'-diphosphoglucose (UDP-Glc) binding subunit of cellulose synthase in Acetobacter xylinum using the photoaffinity probe 5-azido-UDP-Glc. - J. biol. Chem. 265: 4782-4784, 1990. Go to original source...
    63. Little, A., Schwerdt, J.G., Shirley, N.J., Khor, S.F., Neumann, K., O'Donovan, L.A., Lahnstein, J., Collins, H.M., Henderson, M., Fincher, G.B., Burton, R.A.: Revised phylogeny of the cellulose synthase gene superfamily: insights into cell wall evolution. - Plant Physiol. 177: 1124-1141, 2018. Go to original source...
    64. Liu, Z., Schneider, R., Kesten, C., Zhang, Y., Somssich, M., Zhang, Y., Fernie, A.R., Persson, S.: Cellulose-microtubule uncoupling proteins prevent lateral displacement of microtubules during cellulose synthesis in Arabidopsis. - Dev. Cell 38: 305-315, 2016. Go to original source...
    65. Mansoori, N., Timmers, J., Desprez, T., Kamei, C.L.A., Dees, D.C.T., Vincken, J.P., Visser, R.G.F., Hofte, H., Vernhettes, S., Trindade, L.M.: KORRIGAN1 interacts specifically with integral components of the cellulose synthase machinery. - Plos ONE 9: e112387, 2014. Go to original source...
    66. McCarthy, R.L., Zhong, R., Ye, Z.H.: MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. - Plant Cell Physiol. 50: 1950-1964, 2009. Go to original source...
    67. Miart, F., Desprez, T., Biot, E., Morin, H., Belcram, K., Höfte, H., Gonneau, M., Vernhettes, S.: Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis. - Plant J. 77: 71-84, 2014. Go to original source...
    68. Morgan, J.L., Strumillo, J., Zimmer, J.: Crystallographic snapshot of cellulose synthesis and membrane translocation. - Nature 493: 181-186, 2013. Go to original source...
    69. Mølhøj, M., Ulvskov, P., Dal Degan, F.: Characterization of a functional soluble form of a Brassica napus membrane-anchored endo-1,4-β-glucanase heterologously expressed in Pichia pastoris. - Plant Physiol. 127: 674-684, 2001. Go to original source...
    70. Mueller, S.C., Brown, R.M.: Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. - J. Cell Biol. 84: 315-326, 1980. Go to original source...
    71. Nairn, C.J., Haselkorn, T.: Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary cell wall CesA genes of angiosperms. - New Phytol. 166: 907-915, 2005. Go to original source...
    72. Nakagami, H., Sugiyama, N., Mochida, K., Daudi, A., Yoshida, Y., Toyoda, T., Tomita, M., Ishihama, Y., Shirasu, K.: Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. - Plant Physiol. 153: 1161-1174, 2010. Go to original source...
    73. Newman, R.H., Hill, S.J., Harris, P.J.: Wide-angle X-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. - Plant Physiol. 163: 1558-1567, 2013. Go to original source...
    74. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H., Höfte, H.: A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. - EMBO J. 17: 5563-5576, 1998. Go to original source...
    75. Nixon, B.T., Mansouri, K., Singh, A., Du, J., Davis, J.K., Lee, J.G., Slabaugh, E., Vandavasi, V.G., O'Neill, H., Roberts, E.M., Roberts, A.W., Yingling, Y.G., Haigler, C.H.: Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex. - Sci. Rep. 6: 28696, 2016. Go to original source...
    76. Nobles, D.R., Romanovicz, D.K., Brown, R.M., Jr.: Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? - Plant Physiol. 127: 529-542, 2001. Go to original source...
    77. Nühse, T.S., Stensballe, A., Jensen, O.N., Peck, S.C.: Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. - Mol. Cell. Proteomics 2: 1234-1243, 2003. Go to original source...
    78. Oehme, D.P., Downton, M.T., Doblin, M.S., Wagner, J., Gidley, M.J., Bacic, A.: Unique aspects of the structure and dynamics of elementary Iβ cellulose microfibrils revealed by computational simulations. - Plant Physiol. 168: 3-17, 2015. Go to original source...
    79. Pagant, S., Bichet, A., Sugimoto, K., Lerouxel, O., Desprez, T., McCann, M., Lerouge, P., Vernhettes, S., Höfte, H.: KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. - Plant Cell 14: 2001-2013, 2002. Go to original source...
    80. Paredez, A.R., Persson, S., Ehrhardt, D.W., Somerville, C.R.: Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. - Plant Physiol. 147: 1723-1434, 2008. Go to original source...
    81. Paredez, A.R., Somerville, C.R., Ehrhardt, D.W.: Visualization of cellulose synthase demonstrates functional association with microtubules. - Science 312: 1491-1495, 2006. Go to original source...
    82. Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P., Stalker D.M.: Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. - Proc. nat. Acad. Sci. USA 93: 12637-12642, 1996. Go to original source...
    83. Peng, L., Xiang, F., Roberts, E., Kawagoe, Y., Greve, L.C., Kreuz, K., Delmer, D.P.: The experimental herbicide CGA 325'615 inhibits synthesis of crystalline cellulose and causes accumulation of non-crystalline β-1,4-glucan associated with CesA protein. - Plant Physiol. 126: 981-992, 2001. Go to original source...
    84. Peng, L., Zhang, L., Cheng, X., Fan, L.S., Hao, H.Q.: Disruption of cellulose synthesis by 2,6-dichlorobenzonitrile affects the structure of the cytoskeleton and cell wall construction in Arabidopsis. - Plant Biol. 15: 405-414, 2013. Go to original source...
    85. Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Auer, M., Somerville, CR.: Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. - Proc. natl. Acad. Sci. USA 104: 15566-15571, 2007. Go to original source...
    86. Persson, S., Wei, H., Milne, J., Page, G.P., Somerville, C.R.: Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. - Proc. nat. Acad. Sci. USA 102: 8633-8638, 2005. Go to original source...
    87. Polko, J.K., Kieber, J.J.: The regulation of cellulose biosynthesis in plants. - Plant Cell 31: 282-296, 2019. Go to original source...
    88. Ranik, M., Myburg. A.A.: Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. - Tree Physiol. 26: 545-556, 2006. Go to original source...
    89. Richmond, T.A., Somerville, C.R.: The cellulose synthase superfamily. - Plant Physiol. 124: 495-498, 2000. Go to original source...
    90. Robert, S., Bichet, A., Grandjean, O., Kierzkowski, K., Satiat-Jeunemaître, B., Pelletier, S., Hauser, M.T., Höfte, H., Vernhettes, S.: An Arabidopsis endo-1,4-β-D-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. - Plant Cell 17: 3378-3389, 2005. Go to original source...
    91. Roberts, A.W., Bushoven, J.T.: The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens. - Plant mol. Biol. 63: 207-219, 2007. Go to original source...
    92. Roberts, A.W., Roberts, E.M.: Evolution of the cellulose synthase (CesA) gene family: insights from green algae and seedless plants. In: Brown, R.M., Saxena, I.M. (ed.): Cellulose:Mmolecular and Structural Biology. Pp. 17-34. Springer, Dordrecht 2007. Go to original source...
    93. Roberts, E.M., Roberts, A.W.: A cellulose synthase (CESA) gene from the red alga Porphyra yezoensis (Rhodophyta). - J. Phycol. 45: 203-212, 2009. Go to original source...
    94. Ross, P., Mayer, R., Benziman, M.: Cellulose biosynthesis and function in bacteria. - Microbiol. Rev. 55: 35-58, 1991. Go to original source...
    95. Roudier, F., Fernandez, A.G., Fujita, M., Himmelspach, R., Borner, G.H., Schindelman, G., Song, S., Baskin, T.I., Dupree, P., Wasteneys, G.O., Benfey, P.N.: COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. - Plant Cell 17: 1749-1763, 2005. Go to original source...
    96. Sánchez-Rodríguez, C., Bauer, S., Hématy, K., Saxe, F., Ibáñez, A.B., Vodermaier, V., Konlechner, C., Sampathkumar, A., Rüggeberg, M., Aichinger, E., Neumetzler, L., Burgert, I., Somerville, C., Hauser, M.T., Persson, S.: CHITINASE-LIKE1/POM-POM1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. - Plant Cell 24: 589-607, 2012. Go to original source...
    97. Satiat-Jeunemaitre, B.: Spatial and temporal regulations in helicoidal extracellular matrices: comparison between plant and animal systems. - Tissue Cell 24: 315-334, 1992. Go to original source...
    98. Saxena, I.M., Brown, R.M., Jr.: Identification of cellulose synthase(s) in higher plants: sequence analysis of processive β-glycosyltransferases with the common motif 'D, D, D35Q(R,Q)XRW'. - Cellulose 4: 33-49, 1997. Go to original source...
    99. Saxena, I.M., Lin, F.C., Brown, R.M. Jr.: Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. - Plant mol. Biol. 15: 673-683, 1990. Go to original source...
    100. Scheible, W.R., Eshed, R., Richmond, T., Delmer, D., Somerville, C.: Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. - Proc. nat. Acad. Sci. USA 98: 10079-10084, 2001. Go to original source...
    101. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P., McCann, M.C., Benfey, P.N.: COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. - Genes Dev. 15: 1115-1127, 2001. Go to original source...
    102. Sethaphong, L., Davis, J.K., Slabaugh, E., Singh, A., Haigler, C.H.: Prediction of the structures of the plant-specific regions of vascular plant cellulose synthases and correlated functional analysis. - Cellulose 23: 145-161, 2016. Go to original source...
    103. Sethaphong, L., Haigler, C.H., Kubicki, J.D., Zimmer, J., Bonetta, D., De Bolt, S., Yingling, Y.G.: Tertiary model of a plant cellulose synthase. - Proc. nat. Acad. Sci. USA 110: 7512-7517, 2013. Go to original source...
    104. Shaw, S.L., Kamyar, R., Ehrhardt, D.W.: Sustained microtubule treadmilling in Arabidopsis cortical arrays. - Science 300: 1715-1718, 2003. Go to original source...
    105. Slabaugh, E., Davis, J.K., Haigler, C.H., Yingling, Y.G., Zimmer, J.: Cellulose synthases: new insights from crystallography and modeling. - Trends Plant Sci. 19: 99-106, 2014. Go to original source...
    106. Speicher, T.L., Li, P.Z., Wallace, I.S.: Phosphoregulation of the plant cellulose synthase complex and cellulose synthase-like proteins. - Plants (Basel) 7: 52, 2018. Go to original source...
    107. Sullivan, S., Ralet, M.C., Berger, A., Diatloff, E., Bischoff, V., Gonneau, M., Marion-Poll, A., North, H.M.: CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis seeds. - Plant Physiol. 156: 1725-1739, 2011. Go to original source...
    108. Szyjanowicz, P.M., McKinnon, I., Taylor, N.G., Gardiner, J., Jarvis, M.C., Turner, S.R.: The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. - Plant J. 37: 730-740, 2004. Go to original source...
    109. Tanaka, K., Murata, K., Yamazaki, M., Onosato, K., Miyao, A., Hirochika, H.: Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. - Plant Physiol. 133: 73-83, 2003. Go to original source...
    110. Taylor, N.G.: Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites - a potential role in regulating protein degradation. - Plant mol. Biol. 64: 161-171, 2007. Go to original source...
    111. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., Turner, S.R.: Interactions among three distinct CesA proteins essential for cellulose synthesis. - Proc. nat. Acad. Sci. USA 100: 1450-1455, 2003. Go to original source...
    112. Thomas, L.H., Forsyth, V.T., Sturcová, A., Kennedy, C.J., May, R.P., Altaner, C.M., Apperley, D.C., Wess, T.J., Jarvis, M.C.: Structure of cellulose microfibrils in primary cell walls from collenchyma. - Plant Physiol. 161: 465-476, 2013. Go to original source...
    113. Timmers, J., Vernhettes, S., Desprez, T., Vincken, J.P., Visser, R.G., Trindade, L.M.: Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall. - FEBS Lett. 583: 978-982, 2009. Go to original source...
    114. Tsekos, I.: The sites of cellulose synthesis in algae: diversity and evolution of cellulose-synthesizing enzyme complexes. - J. Phycol. 35: 635-655, 1999. Go to original source...
    115. Turner, S.R., Somerville, C.R.: Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. - Plant Cell 9: 689-701, 1997. Go to original source...
    116. Vain, T., Crowell, E.F., Timpano, H., Biot, E., Desprez, T., Mansoori, N., Trindade, L.M., Pagant, S., Robert, S., Höfte, H., Gonneau, M., Vernhettes, S.: The cellulase KORRIGAN is part of the cellulose synthase complex. - Plant Physiol. 165: 1521-1532, 2014. Go to original source...
    117. Vandavasi, V.G., Putnam, D.K., Zhang, Q., Petridis, L., Heller, W.T., Nixon, B.T., Haigler, C.H., Kalluri, U., Coates, L., Langan, P., Smith, J.C., Meiler, J., O'Neill, H.: A structural study of CESA1 catalytic domain of Arabidopsis cellulose synthesis complex: evidence for CESA trimers. - Plant Physiol. 170: 123-135, 2016. Go to original source...
    118. Vanholme, B., Desmet, T., Ronsse, F., Rabaey, K., Van Breusegem, F., De Mey, M., Soetaert, W., Boerjan, W.: Towards a carbon-negative sustainable bio-based economy. - Front. Plant Sci. 4: 174, 2013. Go to original source...
    119. Vergara, C.E., Carpita, N.C.: β-D-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3),(1→4)β-D-glucan synthase. - Plant mol. Biol. 47: 145-160, 2001. Go to original source...
    120. Viëtor, R.J., Newman, R.H., Ha, M.A., Apperley, D.C., Jarvis, M.C.: Conformational features of crystal-surface cellulose from higher plants. - Plant J. 30: 721-731, 2002.
    121. Wang, J., Elliott, J.E., Williamson, R.E.: Features of the primary wall CESA complex in wild type and cellulose-deficient mutants of Arabidopsis thaliana. - J. exp. Bot. 59: 2627-2637, 2008. Go to original source...
    122. Wang, J., Howles, P.A., Cork, A.H., Birch, R.J., Williamson, R.E.: Chimeric proteins suggest that the catalytic and/or C-terminal domains give CesA1 and CesA3 access to their specific sites in the cellulose synthase of primary walls. - Plant Physiol. 142: 685-695, 2006. Go to original source...
    123. Wang, C., Li, J., Yuan, M.: Salt tolerance requires cortical microtubule reorganization in Arabidopsis. - Plant Cell Physiol. 48: 1534-1547, 2007. Go to original source...
    124. Wang, T., McFarlane, H.E., Persson, S.: The impact of abiotic factors on cellulose synthesis. - J. exp. Bot. 67: 543-552, 2016. Go to original source...
    125. Watanabe, Y., Meents, M.J., McDonnell, L.M., Barkwill, S., Sampathkumar, A., Cartwright, H.N., Demura, T., Ehrhardt, D.W., Samuels, A.L., Mansfield, S.D.: Visualization of cellulose synthases in Arabidopsis secondary cell walls. - Science 350: 198-203, 2015. Go to original source...
    126. Wightman, R., Turner, S.: Trafficking of the plant cellulose synthase complex. - Plant Physiol. 153: 427-432, 2010. Go to original source...
    127. Wong, H.C., Fear, A.L., Calhoon, R.D., Eichinger, G.H., Mayer, R., Amikam, D., Benziman, M., Gelfand, D.H., Meade, J.H., Emerick, A.W., Bruner, R., Ben-Bassat, A., Tal, R.: Genetic organization of the cellulose synthase operon in Acetobacter xylinum. - Proc. nat. Acad. Sci. USA 87: 8130-8134, 1990. Go to original source...
    128. Xie, L., Yang, C., Wang, X.: Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. - J. exp. Bot. 62: 4495-4506, 2011. Go to original source...
    129. Zhang, T., Mahgsoudy-Louyeh, S., Tittmann, B., Cosgrove, D.J.: Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis. - Cellulose 21: 853-862, 2014. Go to original source...
    130. Zhang, Y., Nikolovski, N., Sorieul, M., Vellosillo, T., McFarlane, H.E., Dupree, R., Kesten, C., Schneider, R., Driemeier, C., Lathe, R., Lampugnani, E., Yu, X., Ivakov, A., Doblin, M.S., Mortimer, J.C., Brown, S.P., Persson, S., Dupree, P.: Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis. - Nat. Commun. 7: 11656, 2016. Go to original source...
    131. Zhong, R., Lee, C., Ye, Z.H.: Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. - Trends Plant Sci. 15: 625-632, 2010. Go to original source...
    132. Zhong, R., Ye, Z.H.: MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. - Plant Cell Physiol. 53: 368-380, 2012. Go to original source...
    133. Zhu, X., Li, S., Pan, S., Xin, X., Gu, Y.: CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane. - Proc. nat. Acad. Sci. USA 115: E3578-E3587, 2018. Go to original source...
    134. Zuo, J., Niu, Q.W., Nishizawa, N., Wu, Y., Kost, B., Chua, N.H.: KORRIGAN, an Arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. - Plant Cell 12: 1137-1152, 2000. Go to original source...

    Return to the content