The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers

Plant Cell

Volumn 26, Issue 7, 2014, Pages 2996-3009

  Olek, Anna T ^a   Rayon, Catherine ^a,h   Makowski, Lee ^b,c   Kim, Hyung Rae ^d   Ciesielski, Peter ^e   Badger, John ^f   Paul, Lake N ^a   Ghosh, Subhangi ^d   Kihara, Daisuke ^d,g   Crowley, Michael ^e   Himmel, Michael E ^e   Bolin, Jeffrey T ^d   Carpita, Nicholas C ^a,d  

^a PURDUE UNIVERSITY   (United States)

^b Northeastern University   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^f DeltaG Technologies   (United States)

^g Purdue University   (United States)

^h UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; CELLULOSE SYNTHASE; GLUCOSYLTRANSFERASE; PLANT PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN;

CELL MEMBRANE; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; ORYZA; PROTEIN MULTIMERIZATION;

CATALYTIC DOMAIN; CELL MEMBRANE; CELL WALL; CELLULOSE; GLUCOSYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; ORYZA; PLANT PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84907358414     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.126862     Document Type: Article

References (74)

1. Allaire, M., and Yang, L. (2011). Biomolecular solution x-ray scattering at the National Synchrotron Light Source. J. Synchrotron Radiat. 18: 41-44.
2. Atanassov, I.I., Pittman, J.K., and Turner, S.R. (2009). Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Arabidopsis secondary cell walls. J. Biol. Chem. 284: 3833-3841.
3. Atmodjo, M.A., Sakuragi, Y., Zhu, X., Burrell, A.J., Mohanty, S.S., Atwood, J.A., III., Orlando, R., Scheller, H.V., and Mohnen, D. (2011). Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc. Natl. Acad. Sci. USA 108: 20225-20230.
4. Benedetti, M., Leggio, C., Federici, L., De Lorenzo, G., Pavel, N.V., and Cervone, F. (2011). Structural resolution of the complex between a fungal polygalacturonase and a plant polygalacturonase-inhibiting protein by small-angle X-ray scattering. Plant Physiol. 157: 599-607.
5. Benkert, P., Künzli, M., and Schwede, T. (2009). QMEAN server for protein model quality estimation. Nucleic Acids Res. 37: W510-W514.
6. Bilecen, K., Ozturk, U.H., Duru, A.D., Sutlu, T., Petoukhov, M.V., Svergun, D.I., Koch, M.H., Sezerman, U.O., Cakmak, I., and Sayers, Z. (2005). Triticum durum metallothionein. Isolation of the gene and structural characterization of the protein using solution scattering and molecular modeling. J. Biol. Chem. 280: 13701-13711.
7. Bowling, A.J., and Brown, R.M., Jr., (2008). The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. Protoplasma 233: 115-127.
8. Carpita, N.C. (2011). Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1->4)-β-Dglycans. Plant Physiol. 155: 171-184.
9. Charnock, S.J., and Davies, G.J. (1999). Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38: 6380-6385.
10. Currie, M.A., Cameron, K., Dias, F.M.V., Spencer, H.L., Bayer, E.A., Fontes, C.M.G.A., Smith, S.P., and Jia, Z. (2013). Small angle X-ray scattering analysis of Clostridium thermocellum cellulosome N-terminal complexes reveals a highly dynamic structure. J. Biol. Chem. 288: 7978-7985.
11. Daily, M.D., Makowski, L., and Phillips, G.N., Jr., and Cui, Q. (2012). Large-scale motions in the adenylate kinase solution ensemble: coarse-grained simulations and comparison with solution X-ray scattering. Chem. Phys. 396: 84-91.
12. DeLano, W.L. (2002). The PyMOL Molecular Graphics System. (San Carlos, CA: DeLano Scientific).
13. Delmer, D.P. (1999). Cellulose biosynthesis: exciting times for a difficult field of study. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 245-276.
14. 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.
15. Doblin, M.S., Pettolino, F.A., Wilson, S.M., Campbell, R., Burton, R.A., Fincher, G.B., Newbigin, E., and Bacic, A. (2009). A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-β-D-glucan synthesis in transgenic Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 5996-6001.
16. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797.
17. Erickson, H.P. (2009). Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol. Proced. Online 11: 32-51.
18. 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.
19. Gerstein, M., Lesk, A.M., and Chothia, C. (1994). Structural mechanisms for domain movements in proteins. Biochemistry 33: 6739-6749.
20. 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.
21. Grant, T.D., Luft, J.R., Wolfley, J.R., Tsuruta, H., Martel, A., Montelione, G.T., and Snell, E.H. (2011). Small angle X-ray scattering as a complementary tool for high-throughput structural studies. Biopolymers 95: 517-530.
22. 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.
23. Holm, L., and Rosenström, P. (2010). Dali server: conservation mapping in 3D. Nucleic Acids Res. 38: W545-W549.
24. Hura, G.L., et al. (2009). Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat. Methods 6: 606-612.
25. Kelley, L.A., and Sternberg, M.J.E. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4: 363-371.
26. Kezuka, Y., Kojima, M., Mizuno, R., Suzuki, K., Watanabe, T., and Nonaka, T. (2010). Structure of full-length class I chitinase from rice revealed by X-ray crystallography and small-angle X-ray scattering. Proteins 78: 2295-2305.
27. Kolinski, A. (2004). Protein modeling and structure prediction with a reduced representation. Acta Biochim. Pol. 51: 349-371.
28. Kolinski, A., and Bujnicki, J.M. (2005). Generalized protein structure prediction based on combination of fold-recognition with de novo folding and evaluation of models. Proteins 61 (suppl. 7): 84-90.
29. Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J., and Svergun, D.I. (2003). PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36: 1277-1282.
30. Konarev, P.V., Petoukhov, M.V., Volkov, V.V., and Svergun, D.I. (2006). ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39: 277-286.
31. Kozin, M.B., and Svergun, D.I. (2001). Automated matching of high-and low-resolution structural models. J. Appl. Crystallogr. 34: 33-41.
32. Kurek, I., Kawagoe, Y., Jacob-Wilk, D., Doblin, M., and Delmer, D. (2002). Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc. Natl. Acad. Sci. USA 99: 11109-11114.
33. Lamb, J.S., Zoltowski, B.D., Pabit, S.A., Li, L., Crane, B.R., and Pollack, L. (2009). Illuminating solution responses of a LOV domain protein with photocoupled small-angle X-ray scattering. J. Mol. Biol. 393: 909-919.
34. Lee, C., Zhong, R., and Ye, Z.H. (2012). Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone. Plant Cell Physiol. 53: 135-143.
35. Lieth, H. (1975). Primary production of the major vegetation units of the world. In Primary Productivity of the Biosphere, H. Lieth and R.H. Whittaker, eds (New York: Springer-Verlag), pp. 203-215.
36. Linder, M., and Teeri, T.T. (1997). The roles and function of cellulosebinding domains. J. Biotechnol. 57: 15-28.
37. McGuffin, L.J. (2007). Benchmarking consensus model quality assessment for protein fold recognition. BMC Bioinformatics 8: 345.
38. Minh, D.D., and Makowski, L. (2013). Wide-angle X-ray solution scattering for protein-ligand binding: multivariate curve resolution with Bayesian confidence intervals. Biophys. J. 104: 873-883.
39. Morgan, J.L.W., Strumillo, J., and Zimmer, J. (2013). Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493: 181-186.
40. 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.
41. Nishimura, N., Hitomi, K., Arvai, A.S., Rambo, R.P., Hitomi, C., Cutler, S.R., Schroeder, J.I., and Getzoff, E.D. (2009). Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326: 1373-1379.
42. Osawa, T., Sugiura, N., Shimada, H., Hirooka, R., Tsuji, A., Shirakawa, T., Fukuyama, K., Kimura, M., Kimata, K., and Kakuta, Y. (2009). Crystal structure of chondroitin polymerase from Escherichia coli K4. Biochem. Biophys. Res. Commun. 378: 10-14.
43. Palani, K., Kumaran, D., Burley, S.K., and Swaminathan, S. (2011). Crystal structure of a putative glycosyltransferase from Bacteroides fragilis. Protein Data Bank: 3BCV. (http://www.rcsb.org/pdb/explore/ explore.do?structureId=3BCV).
44. Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P., and Stalker, D.M. (1996). Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl. Acad. Sci. USA 93: 12637-12642.
45. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
46. Rossmann, M.G., Moras, D., and Olsen, K.W. (1974). Chemical and biological evolution of nucleotide-binding protein. Nature 250: 194-199.
47. Roy, A., Kucukural, A., and Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5: 725-738.
48. Sali, A., and Blundell, T.L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234: 779-815.
49. Saxena, I.M., Lin, F.C., and Brown, R.M., Jr., (1990). Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol. Biol. 15: 673-683.
50. Saxena, I.M., Brown, R.M., Jr., Fevre, M., Geremia, R.A., and Henrissat, B. (1995). Multidomain architecture of β-glycosyl transferases: implications for mechanism of action. J. Bacteriol. 177: 1419-1424.
51. Saxena, I.M., and Brown, R.M., Jr., and Dandekar, T. (2001). Structurefunction characterization of cellulose synthase: relationship to other glycosyltransferases. Phytochemistry 57: 1135-1148.
52. Schuck, P. (2000). Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78: 1606-1619.
53. Sethaphong, L., Haigler, C.H., Kubicki, J.D., Zimmer, J., Bonetta, D., DeBolt, S., and Yingling, Y.G. (2013). Tertiary model of a plant cellulose synthase. Proc. Natl. Acad. Sci. USA 110: 7512-7517.
54. Shi, J., Blundell, T.L., and Mizuguchi, K. (2001). FUGUE: sequencestructure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310: 243-257.
55. Söding, J., Biegert, A., and Lupas, A.N. (2005). The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33: W244-W248.
56. Svergun, D.I. (1992). Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25: 495-503.
57. Svergun, D.I., and Koch, M.H.J. (2003). Small-angle scattering studies of biological macromolecules in solution. Rep. Prog. Phys. 66: 1735-1782.
58. Svergun, D.I., Volkov, V.V., Kozin, M.B., and Stuhrmann, H.B. (1996). New developments in direct shape determination from small-angle scattering. 2. Uniqueness. Acta Crystallogr. A 52: 419-426.
59. Svergun, D.I., Petoukhov, M.V., and Koch, M.H.J. (2001). Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80: 2946-2953.
60. Taylor, N.G. (2008). Cellulose biosynthesis and deposition in higher plants. New Phytol. 178: 239-252.
61. 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. USA 100: 1450-1455.
62. Taylor, N.G., Gardiner, J.C., Whiteman, R., and Turner, S.R. (2004). Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose 11: 329-338.
63. UniProt Consortium (2013). Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41: D43-D47.
64. Vergara, C.E., and Carpita, N.C. (2001). 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.
65. Wallner, B., and Elofsson, A. (2006). Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci. 15: 900-913.
66. Wang, J., Howles, P.A., Cork, A.H., Birch, R.J., and Williamson, R.E. (2006). 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.
67. Wang, J., Elliott, J.E., and Williamson, R.E. (2008). Features of the primary wall CESA complex in wild type and cellulose-deficient mutants of Arabidopsis thaliana. J. Exp. Bot. 59: 2627-2637.
68. Williamson, T.E., Craig, B.A., Kondrashkina, E., Bailey-Kellogg, C., and Friedman, A.M. (2008). Analysis of self-associating proteins by singular value decomposition of solution scattering data. Biophys. J. 94: 4906-4923.
69. Wong, H.C., et al. (1990). Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc. Natl. Acad. Sci. USA 87: 8130-8134.
70. Wu, S., and Zhang, Y. (2007). LOMETS: a local meta-threading-server for protein structure prediction. Nucleic Acids Res. 35: 3375-3382.
71. Wu, S., and Zhang, Y. (2008). MUSTER: Improving protein sequence profile-profile alignments by using multiple sources of structure information. Proteins 72: 547-556.
72. Yang, Y., Faraggi, E., Zhao, H., and Zhou, Y. (2011). Improving protein fold recognition and template-based modeling by employing probabilistic-based matching between predicted one-dimensional structural properties of query and corresponding native properties of templates. Bioinformatics 27: 2076-2082.
73. Zhang, Y., and Skolnick, J. (2005). TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33: 2302-2309.
74. Zemla, A. (2003). LGA: A method for finding 3D similarities in protein structures. Nucleic Acids Res. 31: 3370-3374.