Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases

Plant Journal

Volumn 89, Issue 4, 2017, Pages 651-670

  McGregor, Nicholas ^a,b   Yin, Victor ^a,b   Tung, Ching Chieh ^b   Van Petegem, Filip ^b   Brumer, Harry ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

licheninase; mixed linkage endoglucanase; Vitis vinifera; X ray crystallography; xyloglucan

Indexed keywords

BACTERIA; BIOLOGY; CRYSTALLOGRAPHY; ENZYME KINETICS; ENZYMES; GENES; PLANT CELL CULTURE; PLANTS (BOTANY); POLYMERS; SINGLE CRYSTALS;

ENDOGLUCANASES; GLYCOSIDE HYDROLASE FAMILY 16; LICHENINASE; STRUCTURAL CHARACTERIZATION; STRUCTURAL COMPARISON; VITIS VINIFERA; X RAY CRYSTAL STRUCTURES; XYLOGLUCANS;

X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY; ENZYMES; GENES; PLANTS;

GLUCAN; GLYCOSYLTRANSFERASE; HYDROLASE; OLIGOSACCHARIDE; PLANT PROTEIN; POLYSACCHARIDE; XYLAN; XYLOGLUCAN; XYLOGLUCAN ENDOTRANSGLYCOSYLASE;

AMINO ACID SEQUENCE; CELL WALL; CHEMISTRY; CRYSTALLOGRAPHY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PROCEDURES; SEQUENCE HOMOLOGY; VITIS;

AMINO ACID SEQUENCE; CELL WALL; CRYSTALLOGRAPHY; EVOLUTION, MOLECULAR; GLUCANS; GLYCOSYLTRANSFERASES; HYDROLASES; OLIGOSACCHARIDES; PHYLOGENY; PLANT PROTEINS; POLYSACCHARIDES; SEQUENCE HOMOLOGY, AMINO ACID; VITIS; XYLANS;

EID: 85012992198     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13421     Document Type: Article

References (94)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221.
2. Afonine, P.V., Grosse-Kunstleve, R.W., Echols, N., Headd, J.J., Moriarty, N.W., Mustyakimov, M., Terwilliger, T.C., Urzhumtsev, A., Zwart, P.H. and Adams, P.D. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352–367.
3. Agirre, J., Iglesias-Fernández, J., Rovira, C., Davies, G.J., Wilson, K.S. and Cowtan, K.D. (2015) Privateer: software for the conformational validation of carbohydrate structures. Nat. Struct. Mol. Biol. 22, 833–834.
4. Albersheim, P., Darvill, A., Roberts, K., Sederoff, R. and Staehelin, A. (2010) Plant Cell Walls. New York, NY: Garland Science.
5. Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V. and Notredame, C. (2006) Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucl. Acids Res. 34, W604–W608.
6. Arnal, G., Attia, M., Asohan, J. and Brumer, H. (2016) A low-volume, parallel copper-bicinchoninic acid (BCA) assay for glycoside hydrolases. In Methods in Molecular Biology, Protein-Carbohydrate Interactions (Lammerts van Bueren, A., and Wade Abbott, D., ed.) New York: Springer (in press, DOI:10.1007/978-1-4939-6899-2_1).
7. Arpat, A.B., Waugh, M., Sullivan, J.P., Gonzales, M., Frisch, D., Main, D., Wood, T., Leslie, A., Wing, R.A. and Wilkins, T.A. (2004) Functional genomics of cell elongation in developing cotton fibers. Plant Mol. Biol. 54, 911–929.
8. Attia, M.A. and Brumer, H. (2016) Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan. Curr. Opin. Struct. Biol. 40, 43–53.
9. Barbeyron, T., Gerard, A., Potin, P., Henrissat, B. and Kloareg, B. (1998) The kappa-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol. Biol. Evol. 15, 528–537.
10. Baumann, M.J., Eklof, J.M., Michel, G., Kallas, A.M., Teeri, T.T., Czjzek, M. and Brumer, H. (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. Plant Cell, 19, 1947–1963.
11. Becnel, J., Natarajan, M., Kipp, A. and Braam, J. (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol. Biol. 61, 451–467.
12. Bourquin, V., Nishikubo, N., Abe, H., Brumer, H., Denman, S., Eklund, M., Christiernin, M., Teeri, T.T., Sundberg, B. and Mellerowicz, E.J. (2002) Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell, 14, 3073–3088.
13. Buchanan, M., Burton, R.A., Dhugga, K.S., Rafalski, A.J., Tingey, S.V., Shirley, N.J. and Fincher, G.B. (2012) Endo-(1,4)-beta-glucanase gene families in the grasses: temporal and spatial co-transcription of orthologous genes. BMC Plant Biol. 12, 19.
14. Burton, R.A., Gidley, M.J. and Fincher, G.B. (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat. Chem. Biol. 6, 724–732.
15. Carpita, N.C. and McCann, M.C. (2000) The cell wall. In Biochemistry and Molecular Biology of Plants (Buchanan, B.B., Guissem, W. and Jones, R.L., eds). Somerset, NJ: John Wiley & Sons Inc, pp. 55–108.
16. Castro, E.d., Sigrist, C.J.A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P.S., Gasteiger, E., Bairoch, A. and Hulo, N. (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucl. Acids Res. 34, W362–W365.
17. Chen, V.B., Arendall, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12–21.
18. Davies, G.J., Wilson, K.S. and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557–559.
19. Eklöf, J.M. and Brumer, H. (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol. 153, 456–466.
20. Eklöf, J.M., Ruda, M.C. and Brumer, H. (2012) Distinguishing xyloglucanase activity in endo-β(1→4)glucanases. Meth. Enzymol. 510, 97–120.
21. Eklöf, J.M., Shojania, S., Okon, M., McIntosh, L.P. and Brumer, H. (2013) Structure-function analysis of a broad specificity Populus trichocarpa endo-β-glucanase reveals an evolutionary link between bacterial licheninases and plant XTH gene products. J. Biol. Chem. 288, 15786–15799.
22. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132.
23. Fenger, T.H. and Brumer, H. (2015) Synthesis and analysis of specific covalent inhibitors of endo-xyloglucanases. ChemBioChem, 16, 575–583.
24. Fibriansah, G., Masuda, S., Koizumi, N., Nakamura, S. and Kumasaka, T. (2007) The 1.3 Å crystal structure of a novel endo-β-1,3-glucanase of glycoside hydrolase family 16 from alkaliphilic Nocardiopsis sp. strain F96. Proteins, 69, 683–690.
25. Fincher, G.B. (2009) Exploring the evolution of (1,3;1,4)-β-D-glucans in plant cell walls: comparative genomics can help!. Curr. Opin. Plant Biol. 12, 140–147.
26. Forment, J., Gadea, J., Huerta, L. et al. (2005) Development of a citrus genome-wide EST collection and cDNA microarray as resources for genomic studies. Plant Mol. Biol. 57, 375–391.
27. Frankova, L. and Fry, S.C. (2013) Biochemistry and physiological roles of enzymes that cut and paste plant cell-wall polysaccharides. J. Exp. Bot. 64, 3519–3550.
28. Fry, S.C., Nesselrode, B.H.W.A., Miller, J.G. and Mewburn, B.R. (2008) Mixed-linkage (1→3,1→4)-β-D-glucan is a major hemicellulose of Equisetum (horsetail) cell walls. New Phytol. 179, 104–115.
29. Fujii, Y. (1999) Crystal structure of an IRF-DNA complex reveals novel DNA recognition and cooperative binding to a tandem repeat of core sequences. EMBO J. 18, 5028–5041.
30. Gaiser, O.J., Piotukh, K., Ponnuswamy, M.N., Planas, A., Borriss, R. and Heinemann, U. (2006) Structural basis for the substrate specificity of a Bacillus 1,3-1,4-β-Glucanase. J. Mol. Biol. 357, 1211–1225.
31. Geisler-Lee, J., Geisler, M., Coutinho, P.M. et al. (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol. 140, 946–962.
32. Gerttula, S., Zinkgraf, M., Muday, G.K., Lewis, D.R., Ibatullin, F.M., Brumer, H., Hart, F., Mansfield, S.D., Filkov, V. and Groover, A. (2015) Transcriptional and hormonal regulation of gravitropism of woody stems in populus. Plant Cell, 27, 2800–2813.
33. Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C.A. and Smith, H.O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Meth, 6, 343–345.
34. Gloster, T.M., Ibatullin, F.M., Macauley, K. et al. (2007) Characterization and Three-dimensional structures of two distinct bacterial xyloglucanases from families GH5 and GH12. J. Biol. Chem. 282, 19177–19189.
35. Goodstein, D.M., Shu, S.Q., Howson, R. et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucl. Acids Res. 40, D1178–D1186.
36. Greer, D.H. and Weston, C. (2010) Heat stress affects flowering, berry growth, sugar accumulation and photosynthesis of Vitis vinifera cv. Semillon grapevines grown in a controlled environment. Funct. Plant Biol. 37, 206–214.
37. Hara, Y., Yokoyama, R., Osakabe, K., Toki, S. and Nishitani, K. (2014) Function of xyloglucan endotransglucosylase/hydrolases in rice. Ann. Bot. 114, 1309–1318.
38. Hatfield, R.D. and Nevins, D.J. (1987) Hydrolytic activity and substrate specificity of an Endoglucanase from Zea mays seedling cell walls. Plant Physiol. 83, 203–207.
39. Hehemann, J.-H., Correc, G., Thomas, F., Bernard, T., Barbeyron, T., Jam, M., Helbert, W., Michel, G. and Czjzek, M. (2012) Biochemical and structural characterization of the complex agarolytic enzyme system from the marine bacterium Zobellia galactanivorans. J. Biol. Chem. 287, 30571–30584.
40. Henriksson, K., Teleman, A., Suortti, T., Reinikainen, T., Jaskari, J., Teleman, O. and Poutanen, K. (1995) Hydrolysis of barley (1→3), (1→4)-β-d-glucan by a cellobiohydrolase II preparation from Trichoderma reesei. Carbohydr. Polym. 26, 109–119.
41. Hrmova, M., Farkas, V., Lahnstein, J. and Fincher, G.B. (2007) A barley xyloglucan xyloglucosyl transferase covalently links xyloglucan, cellulosic substrates, and (1,3;1,4)-beta-D-glucans. J. Biol. Chem. 282, 12951–12962.
42. Ibatullin, F.M., Baumann, M.J., Greffe, L. and Brumer, H. (2008) Kinetic analyses of retaining endo-(xylo)glucanases from plant and microbial sources using new chromogenic xylogluco-oligosaccharide aryl glycosides. Biochemistry, 47, 7762–7769.
43. Johansson, P., Brumer, H., Baumann, M.J., Kallas, A.M., Henriksson, H., Denman, S.E., Teeri, T.T. and Jones, T.A. (2004) Crystal structures of a poplar xyloglucan endotransglycosylase reveal details of transglycosylation acceptor binding. Plant Cell, 16, 874–886.
44. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125–132.
45. Kaewthai, N., Gendre, D., Eklof, J.M., Ibatullin, F.M., Ezcurra, I., Bhalerao, R.P. and Brumer, H. (2013) Group III-A XTH genes of Arabidopsis encode predominant xyloglucan endohydrolases that are dispensable for normal growth. Plant Physiol. 161, 440–454.
46. Koshland, D.E. (1953) Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28, 416–436.
47. Labourel, A., Jam, M., Jeudy, A., Hehemann, J.-H., Czjzek, M. and Michel, G. (2014) The β-Glucanase ZgLamA from Zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin. J. Biol. Chem. 289, 2027–2042.
48. Langer, G., Cohen, S.X., Lamzin, V.S. and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protocols, 3, 1171–1179.
49. Larsbrink, J., Izumi, A., Ibatullin Farid, M., Nakhai, A., Gilbert Harry, J., Davies Gideon, J. and Brumer, H. (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31 α-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem. J. 436, 567–580.
50. Lee, J., Burns, T.H., Light, G., Sun, Y., Fokar, M., Kasukabe, Y., Fujisawa, K., Maekawa, Y. and Allen, R.D. (2010) Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta, 232, 1191–1205.
51. Lombard, V., Ramulu, H.G., Drula, E., Coutinho, P.M. and Henrissat, B. (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucl. Acids Res. 42, D490–D495.
52. Lopez-Casado, G., Urbanowicz, B.R., Damasceno, C.M.B. and Rose, J.K.C. (2008) Plant glycosyl hydrolases and biofuels: a natural marriage. Curr. Opin. Plant Biol. 11, 329–337.
53. Malet, C., Jimenez-Barbero, J., Bernabe, M., Brosa, C. and Planas, A. (1993) Stereochemical course and structure of the products of the enzymic action of endo-1,3-1,4-beta-D-glucan 4-glucanohydrolase from Bacillus licheniformis. Biochem. J. 296, 753–758.
54. Maris, A., Kaewthai, N., Eklof, J.M., Miller, J.G., Brumer, H., Fry, S.C., Verbelen, J.P. and Vissenberg, K. (2011) Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. J. Exp. Bot. 62, 261–271.
55. Mark, P., Baumann, M.J., Eklöf, J.M., Gullfot, F., Michel, G., Kallas, Å.M., Teeri, T.T., Brumer, H. and Czjzek, M. (2009) Analysis of nasturtium TmNXG1 complexes by crystallography and molecular dynamics provides detailed insight into substrate recognition by family GH16 xyloglucan endo-transglycosylases and endo-hydrolases. Proteins, 75, 820–836.
56. Mark, P., Zhang, Q., Czjzek, M., Brumer, H. and Agren, H. (2011) Molecular dynamics simulations of a branched tetradecasaccharide substrate in the active site of a xyloglucan endo-transglycosylase. Mol. Simul. 37, 1001–1013.
57. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674.
58. 14. J. Biol. Chem. 291, 1175–1197. jbc.M115.691659.
59. McGregor, N., Arnal, G. and Brumer, H. (2016) Quantitative kinetic characterization of glycoside hydrolases using high-performance anion-exchange chromatography (HPAEC). In Methods in Molecular Biology, Protein-Carbohydrate Interactions (Lammerts van Bueren, A., and Wade Abbott, D., eds). New York: Springer (in press, DOI:10.1007/978-1-4939-6899-2_2).
60. McPhillips, T.M., McPhillips, S.E., Chiu, H.-J. et al. (2002) Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J. Synchrotron Radiat. 9, 401–406.
61. Mewalal, R., Mizrachi, E., Mansfield, S.D. and Myburg, A.A. (2014) Cell wall-related proteins of unknown function: missing links in plant cell wall development. Plant Cell Physiol. 55, 1031–1043.
62. Michel, G., Chantalat, L., Duee, E., Barbeyron, T., Henrissat, B., Kloareg, B. and Dideberg, O. (2001) The k-carrageenase of P. carrageenovora features a tunnel-shaped active site: a novel insight in the evolution of clan-B glycoside hydrolases. Structure, 9, 513–525.
63. Minic, Z. and Jouanin, L. (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol. Biochem. 44, 435–449.
64. Murphy, F.V. (1999) The structure of a chromosomal high mobility group protein-DNA complex reveals sequence-neutral mechanisms important for non-sequence-specific DNA recognition. EMBO J. 18, 6610–6618.
65. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240–255.
66. Pannu, N.S., Murshudov, G.N., Dodson, E.J. and Read, R.J. (1998) Incorporation of prior phase information strengthens maximum-likelihood structure refinement. Acta Crystallogr. D Biol. Crystallogr. 54, 1285–1294.
67. Pauly, M. and Keegstra, K. (2016) Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. In Annual Review of Plant Biology, Vol 67 (Merchant, S.S. ed.) Palo Alto: Annual Reviews, pp. 235–259.
68. Pauly, M., Gille, S., Liu, L.F., Mansoori, N., de Souza, A., Schultink, A. and Xiong, G.Y. (2013) Hemicellulose biosynthesis. Planta, 238, 627–642.
69. Peng, F.Y., Reid, K.E., Liao, N. et al. (2007) Generation of ESTs in Vitis vinifera wine grape (Cabernet Sauvignon) and table grape (Muscat Hamburg) and discovery of new candidate genes with potential roles in berry development. Gene, 402, 40–50.
70. Planas, A. (2000) Bacterial 1,3-1,4-β-glucanases: structure, function and protein engineering. Biochim. Biophys. Acta, 1543, 361–382.
71. Robert, X. and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucl. Acids Res. 42, W320–W324.
72. Rose, J.K.C. and Lee, S.J. (2010) Straying off the highway: trafficking of secreted plant proteins and complexity in the plant cell wall proteome. Plant Physiol. 153, 433–436.
73. Rose, J.K.C., Braam, J., Fry, S.C. and Nishitani, K. (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant Cell Physiol. 43, 1421–1435.
74. Sampedro, J., Gianzo, C., Iglesias, N., Guitian, E., Revilla, G. and Zarra, I. (2012) AtBGAL10 Is the main xyloglucan beta-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol. 158, 1146–1157.
75. Scheible, W.R. and Pauly, M. (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr. Opin. Plant Biol. 7, 285–295.
76. Scheller, H.V. and Ulvskov, P. (2010) Hemicelluloses. In Annual Review of Plant Biology, Vol 61 (Merchant, S., Briggs, W.R. and Ort, D. eds). Palo Alto: Annual Reviews, pp. 263–289.
77. Shi, Y., Wang, Y.-F., Jayaraman, L., Yang, H., Massagué, J. and Pavletich, N.P. (1998) Crystal Structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-β signaling. Cell, 94, 585–594.
78. Simmons, T.J., Mohler, K.E., Holland, C., Goubet, F., Franková, L., Houston, D.R., Hudson, A.D., Meulewaeter, F. and Fry, S.C. (2015) Hetero-trans-β-glucanase, an enzyme unique to Equisetum plants, functionalises cellulose. Plant J. 83, 753–769.
79. Spadiut, O., Ibatullin, F.M., Peart, J., Gullfot, F., Martinez-Fleites, C., Ruda, M., Xu, C., Sundqvist, G., Davies, G.J. and Brumer, H. (2011) Building custom polysaccharides in vitro with an efficient, broad-specificity xyloglucan glycosynthase and a fucosyltransferase. J. Am. Chem. Soc. 133, 10892–10900.
80. Stein, N. (2008) CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J. Appl. Crystallogr. 41, 641–643.
81. Sundqvist, G., Stenvall, M., Berglund, H., Ottosson, J. and Brumer, H. (2007) A general, robust method for the quality control of intact proteins using LC–ESI-MS. J. Chromatogr. B, 852, 188–194.
82. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.
83. 6-Tagged TEV Protease. In High Throughput Protein Expression and Purification (Doyle, S.A. ed).New York, NY: Humana Press, pp. 297–307.
84. Tuomivaara, S.T., Yaoi, K., O'Neill, M.A. and York, W.S. (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature. Carbohydr. Res. 402, 56–66.
85. Tyler, L., Bragg, J.N., Wu, J.J., Yang, X.H., Tuskan, G.A. and Vogel, J.P. (2010) Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon. BMC Genom. 11, 21.
86. Vagin, A.A., Steiner, R.A., Lebedev, A.A., Potterton, L., McNicholas, S., Long, F. and Murshudov, G.N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60, 2184–2195.
87. Vasur, J., Kawai, R., Andersson, E., Igarashi, K., Sandgren, M., Samejima, M. and Ståhlberg, J. (2009) X-ray crystal structures of Phanerochaete chrysosporium Laminarinase 16A in complex with products from lichenin and laminarin hydrolysis. FEBS J. 276, 3858–3869.
88. Wakarchuk, W.W., Kilburn, D.G., Jr, Miller, R.C. Jr and Warren, R.A.J. (1986) The molecular cloning and expression of a cellobiase gene from an Agrobacterium in Escherichia coli. Molec. Gen. Genet. 205, 146–152.
89. Winn, M.D., Ballard, C.C., Cowtan, K.D. et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235–242.
90. Ye, X., Yuan, S.H., Guo, H., Chen, F., Tuskan, G.A. and Cheng, Z.M. (2012) Evolution and divergence in the coding and promoter regions of the Populus gene family encoding xyloglucan endotransglycosylase/hydrolases. Tree Genet. Genomes, 8, 177–194.
91. Ye, H., Qinggang, Z., Zhengke, Z., Kun, M., Yali, H., Qiuyan, B., Jiangtao, S. and Jingping, R. (2015) Analysis of xyloglucan endotransglycosylase/hydrolase (XTH) Genes and diverse roles of isoenzymes during persimmon fruit development and postharvest softening. PLoS ONE, 10, e0123668 [0123620 pp.].
92. Yokoyama, R., Uwagaki, Y., Sasaki, H., Harada, T., Hiwatashi, Y., Hasebe, M. and Nishitani, K. (2010) Biological implications of the occurrence of 32 members of the XTH (xyloglucan endotransglucosylase/hydrolase) family of proteins in the bryophyte Physcomitrella patens. Plant J. 64, 645–656.
93. 1H-n.m.r. spectroscopy and fast-atom-bombardment mass spectrometry. Carbohydr. Res. 200, 9–31.
94. Zverlov, V.V. and Velikodvorskaya, G.A. (1990) Cloning the Clostridium thermocellum thermostable laminarinase gene in Escherichia coli: the properties of the enzyme thus produced. Biotechnol. Lett. 12, 811–816.