Structure-function analysis of a broad specificity Populus trichocarpa endo-β-glucanase reveals an evolutionary link between bacterial licheninases and plant XTH gene products

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15786-15799

  Eklöf, Jens M ^a,b   Shojania, Shaheen ^b   Okon, Mark ^c   McIntosh, Lawrence P ^b,c   Brumer, Harry ^a,b,c  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BROAD SPECIFICITIES; C-TERMINAL EXTENSIONS; CATALYTIC FUNCTIONS; GLYCOSIDE HYDROLASE FAMILY 16; MOLECULAR EVOLUTION; PHYLOGENETIC ANALYSIS; POPULUS TRICHOCARPA; STRUCTURE-FUNCTION ANALYSIS;

CATALYSIS; ENZYME ACTIVITY; MOLECULAR BIOLOGY; PLANT CELL CULTURE; PLANTS (BOTANY); POLYMERS;

GENES;

BACTERIAL ENZYME; ENDO BETA GLUCANASE; GLUCAN SYNTHASE; LICHENINASE; UNCLASSIFIED DRUG;

ARTICLE; CLADISTICS; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PLANT GENE; POPULUS TRICHOCARPA; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; XTH GENE;

CARBOHYDRATE PROCESSING; CELLULASE; ENZYME KINETICS; ENZYME STRUCTURE; GLYCOSIDE HYDROLASES; LICHENINASE; PLANT CELL WALL; POLYSACCHARIDE; XYLOGLUCAN; XYLOGLUCAN ENDOTRANSGLYCOSYLASE/HYDROLASE (XTH);

BACTERIAL PROTEINS; CATALYTIC DOMAIN; EVOLUTION, MOLECULAR; GLYCOSIDE HYDROLASES; GLYCOSYLTRANSFERASES; PHYLOGENY; PLANT PROTEINS; POPULUS; PROTEIN STRUCTURE, SECONDARY;

BACTERIA (MICROORGANISMS); POPULUS TRICHOCARPA;

EID: 84878387277     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.462887     Document Type: Article

References (83)

1. Carpita, N., and McCann, M. (2000) The cell wall. in Biochemistry and Molecular Biology of Plants (Buchanan, B., Gruissem, W., and Jones, R., eds) pp. 52-108, John Wiley & Sons, Inc., Somerset, NJ
2. Himmel, M. E., Ding, S. Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., and Foust, T. D. (2007) Biomass recalcitrance. Engineering plants and enzymes for biofuels production. Science 315, 804-807
3. Ragauskas, A. J., Williams, C. K., Davison, B. H., Britovsek, G., Cairney, J., Eckert, C. A., Frederick, W. J., Jr., Hallett, J. P., Leak, D. J., Liotta, C. L., Mielenz, J. R., Murphy, R., Templer, R., and Tschaplinski, T. (2006) The path forward for biofuels and biomaterials. Science 311, 484-489 (Pubitemid 43158454)
4. Cosgrove, D. J. (2005) Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6, 850-861
5. Vogel, J. (2008) Unique aspects of the grass cell wall. Curr. Opin. Plant Biol. 11, 301-307
6. Fangel, J. U., Ulvskov, P., Knox, J. P., Mikkelsen, M. D., Harholt, J., Popper, Z. A., and Willats, W. G. (2012) Cell wall evolution and diversity. Front. Plant Sci. 3, 152
7. Henrissat, B., Coutinho, P. M., and Davies, G. J. (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47, 55-72 (Pubitemid 32817808)
8. Geisler-Lee, J., Geisler, M., Coutinho, P. M., Segerman, B., Nishikubo, N., Takahashi, J., Aspeborg, H., Djerbi, S., Master, E., Andersson- Gunnerås, S., Sundberg, B., Karpinski, S., Teeri, T. T., Kleczkowski, L. A., Henrissat, B., and Mellerowicz, E. J. (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol. 140, 946-962 (Pubitemid 43956248)
9. Yokoyama, R., Rose, J. K., and Nishitani, K. (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol. 134, 1088-1099 (Pubitemid 38398257)
10. Popper, Z. A., Michel, G., Hervé, C., Domozych, D. S., Willats, W. G., Tuohy, M. G., Kloareg, B., and Stengel, D. B. (2011) Evolution and diversity of plant cell walls. From algae to flowering plants. Annu. Rev. Plant Biol. 62, 567-590
11. Baumann, M. J., Eklöf, J. M., Michel, G., Kallas, A. M., Teeri, T. T., Czjzek, M., and Brumer, H., 3rd (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases. Biological implications for cell wall metabolism. Plant Cell 19, 1947-1963 (Pubitemid 47218851)
12. Kaewthai, N., Gendre, D., Eklöf, J. M., Ibatullin, F. M., Ezcurra, I., Bhalerao, R. P., and Brumer, H. (2013) Group III-A XTH genes of Arabidopsis thaliana encode predominant xyloglucan endo-hydrolases that are dispensable for normal growth. Plant Physiol. 161, 440-454
13. 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
14. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy). An expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
15. Michel, G., Chantalat, L., Duee, E., Barbeyron, T., Henrissat, B., Kloareg, B., and Dideberg, O. (2001) The κ-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 (Pubitemid 32575348)
16. Planas, A. (2000) Bacterial 1,3-1,4-β-glucanases. Structure, function, and protein engineering. Biochim. Biophys. Acta 1543, 361-382
17. Davies, G. J., and Sinnott, M. L. (2008) Sorting the diverse. The sequence-based classifications of carbohydrate-active enzymes. Biochem. J., doi: 10.1042/BJ20080382
18. Eklöf, J. M., Ruda, M. C., and Brumer, H. (2012) Distinguishing xyloglucanase activity in endo-β(1→4)glucanases. Methods Enzymol. 510, 97-120
19. Van Sandt, V. S., Stieperaere, H., Guisez, Y., Verbelen, J. P., and Vissenberg, K. (2007) XET activity is found near sites of growth and cell elongation in bryophytes and some green algae. New insights into the evolution of primary cell wall elongation. Ann. Bot. 99, 39-51 (Pubitemid 47355444)
20. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides. SignalP 3.0. J. Mol. Biol. 340, 783-795 (Pubitemid 38829638)
21. Emanuelsson, O., Nielsen, H., and von Heijne, G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8, 978-984 (Pubitemid 29211735)
22. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12, 1652-1662 (Pubitemid 36910046)
23. Hamby, S. E., and Hirst, J. D. (2008) Prediction of glycosylation sites using random forests. BMC Bioinformatics 9, 500
24. Childs, K. L., Hamilton, J. P., Zhu, W., Ly, E., Cheung, F., Wu, H., Rabinowicz, P. D., Town, C. D., Buell, C. R., and Chan, A. P. (2007) The TIGR plant transcript assemblies database. Nucleic Acids Res. 35, D846-D851 (Pubitemid 46056320)
25. Edgar, R. C. (2004) MUSCLE. Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
26. Hall, T. A. (1999) BioEdit. A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98
27. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (Pubitemid 37365050)
28. Huelsenbeck, J. P., and Ronquist, F. (2001) MrBayes. Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755 (Pubitemid 32851390)
29. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4. Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (Pubitemid 47236692)
30. Oganesyan, N., Kim, S. H., and Kim, R. (2005) On-column protein refolding for crystallization. J. Struct. Funct. Genomics 6, 177-182 (Pubitemid 41428126)
31. Czisch, M., and Boelens, R. (1998) Sensitivity enhancement in the TROSY experiment. J. Magn. Reson. 134, 158-160 (Pubitemid 128451268)
32. Meissner, A., Schulte-Herbruggen, T., Briand, J., and Sørensen, O. W. (1998) Double spin-state-selective coherence transfer. Application for two-dimensional selection of multiplet components with long transverse relaxation times. Mol. Phys. 95, 1137-1142 (Pubitemid 128495243)
33. Weigelt, J. (1998) Single scan, sensitivity- and gradient-enhanced TROSY for multidimensional NMR experiments. J. Am. Chem. Soc. 120, 10778-10779
34. Rance, M., Loria, J. P., and Palmer, A. G. (1999) Sensitivity improvement of transverse relaxation-optimized spectroscopy. J. Magn. Reson. 136, 92-101 (Pubitemid 129607251)
35. Zhu, G., Kong, X. M., and Sze, K. H. (1999) Gradient and sensitivity enhancement of 2D TROSY with water flip-back, 3D NOESY-TROSY and TOCSY-TROSY experiments. J. Biomol. NMR 13, 77-81 (Pubitemid 29089243)
36. Eletsky, A., Kienöfer, A., and Pervushin, K. (2001) TROSY NMR with partially deuterated proteins. J. Biomol. NMR 20, 177-180 (Pubitemid 32677761)
37. Salzmann, M., Wider, G., Pervushin, K., Senn, H., and Wüthrich, K. (1999) TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins. J. Am. Chem. Soc. 121, 844-848
38. Salzmann, M., Pervushin, K., Wider, G., Senn, H., and Wüthrich, K. (1998) TROSY in triple-resonance experiments. New perspectives for sequential NMR assignment of large proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 13585-13590 (Pubitemid 28523015)
39. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
40. Godard, T., and Kneller, D. G. (2008) SPARKY version 3.115, University of California, San Francisco
41. Shen, Y., and Bax, A. (2012) Identification of helix capping and β-turn motifs from NMR chemical shifts. J. Biomol. NMR 52, 211-232
42. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+. A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
43. Camilloni, C., De Simone, A., Vranken, W. F., and Vendruscolo, M. (2012) Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 51, 2224-2231
44. Campbell, P., and Braam, J. (1999) In vitro activities of four xyloglucan endotransglycosylases from Arabidopsis. Plant J. 18, 371-382
45. Johansson, P., Brumer, H., 3rd, 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 (Pubitemid 38459208)
46. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., Studholme, D. J., Yeats, C., and Eddy, S. R. (2004) The Pfam protein families database. Nucleic Acids Res. 32, D138-D141 (Pubitemid 38081623)
47. Hahn, M., Pons, J., Planas, A., Querol, E., and Heinemann, U. (1995) Crystal structure of Bacillus licheniformis 1,3-1,4-β-D-glucan 4-glucanohydrolase at 1.8 Å resolution. FEBS Lett. 374, 221-224
48. 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 (Pubitemid 43357982)
49. Del Bem, L. E., and Vincentz, M. G. (2010) Evolution of xyloglucan-related genes in green plants. BMC Evol. Biol. 10, 341
50. 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
51. Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D. S. (2012) Phytozome. A comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186
52. Sørensen, I., Pettolino, F. A., Bacic, A., Ralph, J., Lu, F., O'Neill, M. A., Fei, Z. Z., Rose, J. K., Domozych, D. S., and Willats, W. G. (2011) The charophycean green algae provide insights into the early origins of plant cell walls. Plant J. 68, 201-211
53. McFeeters, R. F. (1980) A manual method for reducing sugar determinations with 2,2′-bicinchoninate reagent. Anal. Biochem. 103, 302-306
54. Nelson, N. (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 153, 375-380
55. Burton, R. A., and Fincher, G. B. (2009) (1,3;1,4)-β-D-Glucans in cell walls of the poaceae, lower plants, and fungi. A tale of two linkages. Mol. Plant. 2, 873-882
56. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559 (Pubitemid 27056509)
57. Fry, S. C., York, W. S., Albersheim, P., Darvill, A., Hayashi, T., Joseleau, J. P., Kato, Y., Lorences, E. P., Maclachlan, G. A., McNeil, M., Mort, A. J., Reid, J. S., Seitz, H. U., Selvendran, R. R., Voragen, A. G., and White, A. R. (1993) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol. Plant. 89, 1-3
58. York, W. S., Harvey, L. K., Guillen, R., Albersheim, P., and Darvill, A. G. (1993) The structure of plant-cell walls. 36. Structural-analysis of tamarind seed xyloglucan oligosaccharides using β-galactosidase digestion and spectroscopic methods. Carbohydr. Res. 248, 285-301 (Pubitemid 23302986)
59. York, W. S., Impallomeni, G., Hisamatsu, M., Albersheim, P., and Darvill, A. G. (1995) 11 newly characterized xyloglucan oligoglycosyl alditols. The specific effects of side-chain structure and location on H-1-NMR chemical-shifts. Carbohydr. Res. 267, 79-104
60. 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)-β-D-glucans. J. Biol. Chem. 282, 12951-12962 (Pubitemid 47100602)
61. Mohler, K. E., Simmons, T. J., and Fry, S. C. (2013) Mixed-linkage glucan: xyloglucan endotransglucosylase (MXE) re-models hemicelluloses in Equisetum shoots but not in barley shoots or Equisetum callus. New Phytol. 197, 111-122
62. Fernandez-Fuentes, N., Madrid-Aliste, C. J., Rai, B. K., Fajardo, J. E., and Fiser, A. (2007) M4T. A comparative protein structure modeling server. Nucleic Acids Res. 35, W363-W368
63. Hahn, M., Keitel, T., and Heinemann, U. (1995) Crystal and molecular-structure at 0.16 nm resolution of the hybrid Bacillus endo-1,3-1,4-β-D-glucan 4-glucanohydrolase H (A16-M). Eur. J. Biochem. 232, 849-858
64. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web. A case study using the Phyre server. Nat. Protoc. 4, 363-371
65. Bahrami, A., Assadi, A. H., Markley, J. L., and Eghbalnia, H. R. (2009) Probabilistic interaction network of evidence algorithm and its application to complete labeling of peak lists from protein NMR spectroscopy. PLoS Comput. Biol. 5, e1000307
66. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222, 311-333 (Pubitemid 121004009)
67. 13C chemical-shift data. J. Biomol. NMR 4, 171-180
68. Marsh, J. A., Singh, V. K., Jia, Z., and Forman-Kay, J. D. (2006) Sensitivity of secondary structural propensities to sequence differences between α- and γ-synuclein. Implications for fibrillation. Protein Sci. 15, 2795-2804 (Pubitemid 44833760)
69. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003) VADAR. A Web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 31, 3316-3319 (Pubitemid 37442148)
70. Wishart, D. S., Arndt, D., Berjanskii, M., Tang, P., Zhou, J., and Lin, G. (2008) CS23D. A Web server for rapid protein structure generation using NMR chemical shifts and sequence data. Nucleic Acids Res. 36, W496-W502
71. Chen, J. H., Tsai, L. C., Huang, H. C., and Shyur, L. F. (2010) Structural and catalytic roles of amino acid residues located at substrate-binding pocket in Fibrobacter succinogenes 1,3-1,4-β-D-glucanase. Proteins 78, 2820-2830
72. Mark, P., Baumann, M. J., Eklöf, J. M., Gullfot, F., Michel, G., Kallas, A. 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
73. 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
74. Addington, T., Calisto, B., Alfonso-Prieto, M., Rovira, C., Fita, I., and Planas, A. (2011) Re-engineering specificity in 1,3-1,4-β-glucanase to accept branched xyloglucan substrates. Proteins 79, 365-375
75. Saura-Valls, M., Fauré, R., Brumer, H., Teeri, T. T., Cottaz, S., Driguez, H., and Planas, A. (2008) Active-site mapping of a Populus xyloglucan endotransglycosylase with a library of xylogluco-oligosaccharides. J. Biol. Chem. 283, 21853-21863
76. Campbell, P., and Braam, J. (1998) Co- and/or post-translational modifications are critical for TCH4 XET activity. Plant J. 15, 553-561
77. Kallas, A. M., Piens, K., Denman, S. E., Henriksson, H., Fäldt, J., Johansson, P., Brumer, H., and Teeri, T. T. (2005) Enzymatic properties of native and deglycosylated hybrid aspen (Populus tremula x tremuloides) xyloglucan endotransglycosylase 16A expressed in Pichia pastoris. Biochem. J. 390, 105-113 (Pubitemid 41192236)
78. Barbeyron, T., Gerard, A., Potin, P., Henrissat, B., and Kloareg, B. (1998) The κ-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol. Biol. Evol. 15, 528-537 (Pubitemid 28194616)
79. Hehemann, J. H., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., and Michel, G. (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908-912
80. 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
81. Domozych, D. S., Ciancia, M., Fangel, J. U., Mikkelsen, M. D., Ulvskov, P., and Willats, W. G. (2012) The cell walls of green algae. A journey through evolution and diversity. Front. Plant Sci. 3, 82
82. 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
83. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript. Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323 (Pubitemid 37442149)