Molecular mechanisms associated with xylan degradation by xanthomonas plant pathogens

Journal of Biological Chemistry

Volumn 289, Issue 46, 2014, Pages 32186-32200

  Santos, Camila Ramos ^a   Hoffmam, Zaira Bruna ^b   De Matos Martins, Vanesa Peixoto ^a   Zanphorlin, Leticia Maria ^b   De Paula Assis, Leandro Henrique ^a   Honorato, Rodrigo Vargas ^a   De Oliveira, Paulo Sérgio Lopes ^a   Ruller, Roberto ^b   Murakami, Mario Tyago ^a  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

MOLECULAR MECHANISM; PHYTOPATHOGENS; PLANT PATHOGEN; STRUCTURAL BASIS; XYLAN DEGRADATIONS; XYLANOLYTIC ACTIVITY; XYLANOLYTIC ENZYMES; XYLOOLIGOSACCHARIDES;

BIOLOGY;

CALCIUM ION; ENDO 1,4 BETA XYLANASE; ENDO BETA 1,4 XYLANASE XYNB; EXOOLIGOXYLANASE XYNA; GLYCOSIDASE; GLYCOSIDE HYDROLASE 10; UNCLASSIFIED DRUG; XYLAN; XYLAN ENDO 1,3 BETA XYLOSIDASE; BACTERIAL PROTEIN; BETA GLUCOSIDASE; CALCIUM; ION; OLIGOSACCHARIDE; XYNB XYLANASE;

ARTICLE; BIOFILM; CELL MEMBRANE PERMEABILITY; CELL WALL; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME REPRESSION; ENZYME STABILITY; ENZYME SUBSTRATE; GENE MUTATION; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PLANT CELL; PLANT GENE; REGULATORY MECHANISM; STATIC ELECTRICITY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VIRULENCE; XANTHOMONAS; XYNA GENE; XYNB GENE; AMINO ACID SEQUENCE; CALORIMETRY; CARBOHYDRATE METABOLISM; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PLANT; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BETA-GLUCOSIDASE; CALCIUM; CALORIMETRY; CARBOHYDRATE METABOLISM; CELL WALL; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ENDO-1,4-BETA XYLANASES; GLYCOSIDE HYDROLASES; IONS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PLANTS; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; XANTHOMONAS; XYLANS;

EID: 84910650613     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.605105     Document Type: Article

References (69)

1. Ray, S. K., Rajeshwari, R., and Sonti, R. V. (2000) Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol. Plant. Microbe Interact. 13, 394-401
2. Hu, J., Qian, W., and He, C. (2007) The Xanthomonas oryzae pv. oryzae eglXoB endoglucanase gene is required for virulence to rice. FEMS Microbiol. Lett. 269, 273-279
3. Rajeshwari, R., Jha, G., and Sonti, R. V. (2005) Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting viru-lence on rice. Mol. Plant. Microbe Interact. 18, 830-837
4. Albersheim, P., Jones, T. M., and English, P. D. (1969) Biochemistry of the cell wall in relation to infective processes. Annu. Rev. Phytopathol. 7, 171-194
5. Büttner, D., and Bonas, U. (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol. Rev. 34, 107-133
6. Preston, G. M., Studholme, D. J., and Caldelari, I. (2005) Profiling the secretomes of plant pathogenic Proteobacteria. FEMS Microbiol. Rev. 29, 331-360
7. Jha, G., Rajeshwari, R., and Sonti, R. V. (2005) Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens. Mol. Plant. Microbe Interact. 18, 891-898
8. Enkerli, J., Felix, G., and Boller, T. (1999) The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol. 121, 391-397
9. Furman-Matarasso, N., Cohen, E., Du, Q., Chejanovsky, N., Hanania, U., and Avni, A. (1999) A point mutation in the ethylene-inducing xylanase elicitor inhibits the beta-1-4-endoxylanase activity but not the elicitation activity. Plant Physiol. 121, 345-351
10. Hanania, U., and Avni, A. (1997) High-affinity binding site for ethyleneinducing xylanase elicitor on Nicotiana tabacum membranes. Plant J. 12, 113-120
11. Ryan, C. A. (1987) Oligosaccharide signalling in plants. Annu. Rev. Cell Biol. 3, 295-317
12. Fry, S. C., Aldington, S., Hetherington, P. R., and Aitken, J. (1993) Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol. 103, 1-5
13. Palva, T. K., Holmstrom, K.-O., Heino, P., and Palva, E. T. (1993) Induction of plant defense response by exoenzymes of Erwinia carotovora subsp. carotovora. Mol. Plant. Microbe Interact. 6, 190-196
14. Szczesny, R., Jordan, M., Schramm, C., Schulz, S., Cogez, V., Bonas, U., and Büttner, D. (2010) Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria. New Phytol. 187, 983-1002
15. Jha, G., Rajeshwari, R., and Sonti, R. V. (2007) Functional interplay between two Xanthomonas oryzae pv,. oryzae secretion systems in modulating virulence on rice. Mol. Plant. Microbe Interact. 20, 31-40
16. Yamazaki, A., Hirata, H., and Tsuyumu, S. (2008) HrpG regulates type II secretory proteins in Xanthomonas axonopodis pv. citri. J. Gen. Plant Pathol. 74, 138-150
17. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495
18. Gottwald, T. R., and Graham, J. H. (1992) A device for precise and nondisruptive stomatal inoculation of leaf tissue with bacterial pathogens. Phytopathology 82, 930-935
19. Graham, J. H., Gottwald, T. R., Riley, T. D., and Achor, D. (1992) Penetration through leaf stomata and strains of Xanthomonas campestris in citrus cultivars varying in susceptibility to bacterial diseases. Phytopathology 82, 1319-1325
20. Déjean, G., Blanvillain-Baufumé, S., Boulanger, A., Darrasse, A., Dugé de Bernonville, T., Girard, A. L., Carrére, S., Jamet, S., Zischek, C., Lautier, M., Solé, M., Büttner, D., Jacques, M. A., Lauber, E., and Arlat, M. (2013) The xylan utilization system of the plant pathogen Xanthomonas campestris pv. campestris controls epiphytic life and reveals common features with oligotrophic bacteria and animal gut symbionts. New Phytol. 198, 899-915
21. Li, J., and Wang, N. (2011) Genome-wide mutagenesis of Xanthomonas axonopodis pv. citri reveals novel genetic determinants and regulation mechanisms of biofilm formation. PLoS One 6, e21804
22. Shibuya, N., and Minami, E. (2001) Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59, 223-233
23. Miller, G. L. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-428
24. Chen, F. T., and Evangelista, R. A. (1995) Analysis of mono-and oligosaccharide isomers derivatized with 9-aminopyrene-1,4,6-trisulfonate by capillary electrophoresis with laser-induced fluorescence. Anal. Biochem. 230, 273-280
25. Keller, S., Vargas, C., Zhao, H., Piszczek, G., Brautigam, C. A., and Schuck, P. (2012) High-precision isothermal titration calorimetry with automated peak-shape analysis. Anal. Chem. 84, 5066-5073
26. Hammersley, A. P., Brown, K., Burmeister, W., Claustre, L., Gonzalez, A., McSweeney, S., Mitchell, E., Moy, J. P., Svensson, S. O., and Thompson, A. W. (1997) Calibration and application of an x-ray image intensifier/ charge-coupled device detector for monochromatic macromolecular crystallography. J. Synchrotron Radiat. 4, 67-77
27. Svergun, D. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
28. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886
29. Volkov, V. V., and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864
30. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773
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. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
33. Kabsch, W. (2010) XDS. Acta Crystallogr. D. Biol. Crystallogr. 66, 125-132
34. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D. Biol. Crystallogr. 66, 479-485
35. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L. W., Read, R. J., and Adams, P. D. (2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D. Biol. Crystallogr. 64, 61-69
36. 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
37. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D. Biol. Crystallogr. 66, 486-501
38. Chen, V. B., Arendall, W. B., 3rd, 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
39. Krieger, E., Koraimann, G., and Vriend, G. (2002) Increasing the precision of comparative models with YASARA NOVA: a self-parameterizing force field. Proteins 47, 393-402
40. Pell, G., Taylor, E. J., Gloster, T. M., Turkenburg, J. P., Fontes, C. M., Ferreira, L. M., Nagy, T., Clark, S. J., Davies, G. J., and Gilbert, H. J. (2004) The mechanisms by which family 10 glycoside hydrolases bind decorated substrates. J. Biol. Chem. 279, 9597-9605
41. Solomon, V., Teplitsky, A., Shulami, S., Zolotnitsky, G., Shoham, Y., and Shoham, G. (2007) Structure-specificity relationships of an intracellular xylanase from Geobacillus stearothermophilus. Acta Crystallogr. D. Biol. Crystallogr. 63, 845-859
42. Gallardo, O., Pastor, F. I., Polaina, J., Diaz, P., Lysek, R., Vogel, P., Isorna, P., González, B., and Sanz-Aparicio, J. (2010) Structural insights into the specificity of Xyn10B from Paenibacillus barcinonensis and its improved stability by forced protein evolution. J. Biol. Chem. 285, 2721-2733
43. Honda, Y., and Kitaoka, M. (2004) A family 8 glycoside hydrolase from Bacillus halodurans C-125 (BH2105) is a reducing end xylose-releasing exo-oligoxylanase. J. Biol. Chem. 279, 55097-55103
44. Fushinobu, S., Hidaka, M., Honda, Y., Wakagi, T., Shoun, H., and Kitaoka, M. (2005) Structural basis for the specificity of the reducing end xylosereleasing exo-oligoxylanase from Bacillus halodurans C-125. J. Biol. Chem. 280, 17180-17186
45. Mirande, C., Mosoni, P., Béra-Maillet, C., Bernalier-Donadille, A., and Forano, E. (2010) Characterization of Xyn10A, a highly active xylanase from the human gut bacterium Bacteroides xylanisolvens XB1A. Appl. Microbiol. Biotechnol. 87, 2097-2105
46. Guo, B., Chen, X. L., Sun, C. Y., Zhou, B. C., and Zhang, Y. Z. (2009) Gene cloning, expression and characterization of a new cold-active and salttolerant endo-1,4-xylanase from marine Glaciecola mesophila KMM 241. Appl. Microbiol. Biotechnol. 84, 1107-1115
47. Fujimoto, Z., Kuno, A., Kaneko, S., Kobayashi, H., Kusakabe, I., and Mizuno, H. (2002) Crystal structures of the sugar complexes of Streptomyces olivaceoviridis E-86 xylanase: sugar binding structure of the family 13 carbohydrate binding module. J. Mol. Biol. 316, 65-78
48. Santos, C. R., Meza, A. N., Hoffmam, Z. B., Silva, J. C., Alvarez, T. M., Ruller, R., Giesel, G. M., Verli, H., Squina, F. M., Prade, R. A., and Murakami, M. T. (2010) Thermal-induced conformational changes in the product release area drive the enzymatic activity of xylanases 10B: crystal structure, conformational stability and functional characterization of the xylanase 10B from Thermotoga petrophila RKU-1. Biochem. Biophys. Res. Commun. 403, 214-219
49. Shi, H., Zhang, Y., Li, X., Huang, Y., Wang, L., Wang, Y., Ding, H., and Wang, F. (2013) A novel highly thermostable xylanase stimulated by Ca2- from Thermotoga thermarum: cloning, expression and characterization. Biotechnol. Biofuels 6, 26
50. Spurway, T. D., Morland, C., Cooper, A., Sumner, I., Hazlewood, G. P., O'Donnell, A. G., Pickersgill, R. W., and Gilbert, H. J. (1997) Calcium protects a mesophilic xylanase from proteinase inactivation and thermal unfolding. J. Biol. Chem. 272, 17523-17530
51. Wang, G., Luo, H., Wang, Y., Huang, H., Shi, P., Yang, P., Meng, K., Bai, Y., and Yao, B. (2011) A novel cold-active xylanase gene from the environmental DNA of goat rumen contents: direct cloning, expression and enzyme characterization. Bioresour. Technol. 102, 3330-3336
52. Zheng, H., Chordia, M. D., Cooper, D. R., Chruszcz, M., Müller, P., Sheldrick, G. M., and Minor, W. (2014) Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server. Nat. Protoc. 9, 156-170
53. Najmudin, S., Pinheiro, B. A., Prates, J. A., Gilbert, H. J., Roma?o, M. J., and Fontes, C. M. (2010) Putting an N-terminal end to the Clostridium thermocellum xylanase Xyn10B story: crystal structure of the CBM22-1-GH10 modules complexed with xylohexaose. J. Struct. Biol. 172, 353-362
54. Grennan, A. K. (2006) Plant response to bacterial pathogens. Overlap between innate and gene-for-gene defense response. Plant Physiol. 142, 809-811
55. Broekaert, W. F., Terras, F. R., Cammue, B. P., and Osborn, R. W. (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108, 1353-1358
56. Veronese, P., Ruiz, M. T., Coca, M. A., Hernandez-Lopez, A., Lee, H., Ibeas, J. I., Damsz, B., Pardo, J. M., Hasegawa, P. M., Bressan, R. A., and Narasimhan, M. L. (2003) In defense against pathogens: both plant sentinels and foot soldiers need to know the enemy. Plant Physiol. 131, 1580-1590
57. Liu, Y., Schiff, M., Czymmek, K., Tallóczy, Z., Levine, B., and Dinesh-Kumar, S. P. (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567-577
58. Van Vu, B., Itoh, K., Nguyen, Q. B., Tosa, Y., and Nakayashiki, H. (2012) Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol. Plant. Microbe Interact. 25, 1135-1141
59. Faure, D. (2002) The family-3 glycoside hydrolases: from housekeeping functions to host-microbe interactions. Appl. Environ. Microbiol. 68, 1485-1490
60. King, B. C., Waxman, K. D., Nenni, N. V., Walker, L. P., Bergstrom, G. C., and Gibson, D. M. (2011) Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol. Biofuels 4, 4
61. Fierens, K., Gils, A., Sansen, S., Brijs, K., Courtin, C. M., Declerck, P. J., De Ranter, C. J., Gebruers, K., Rabijns, A., Robben, J., Campenhout, S., Volckaert, G., and Delcour, J. A. (2005) His374 of wheat endoxylanase inhibitor TAXI-I stabilizes complex formation with glycoside hydrolase family 11 endoxylanases. FEBS J. 272, 5872-5882
62. Yoshizawa, T., Shimizu, T., Hirano, H., Sato, M., and Hashimoto, H. (2012) Structural basis for inhibition of xyloglucan-specific endo-1,4-glucanase (XEG) by XEG-protein inhibitor. J. Biol. Chem. 287, 18710-18716
63. de Jonge, R., van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M. H., and Thomma, B. P. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953-955
64. Schuster, A., and Schmoll, M. (2010) Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 87, 787-799
65. Doran-Peterson, J., Jangid, A., Brandon, S. K., DeCrescenzo-Henriksen, E., Dien, B., and Ingram, L. O. (2009) Simultaneous saccharification and fermentation and partial saccharification and co-fermentation of lignocellulosic biomass for ethanol production. Methods Mol. Biol. 581, 263-280
66. Harris, G. W., Jenkins, J. A., Connerton, I., and Pickersgill, R. W. (1996) Refined crystal structure of the catalytic domain of xylanase A from Pseudomonas fluorescens at 1.8 A resolution. Acta Crystallogr. D. Biol. Crystallogr. 52, 393-401
67. Tina, K. G., Bhadra, R., and Srinivasan, N. (2007) PIC: protein interactions calculator. Nucleic Acids Res. 35, W473-W476
68. Hespell, R. B., and Cotta, M. A. (1995) Degradation and utilization by Butyrivibrio fibrisolvens H17c of xylans with different chemical and physical properties. Appl. Environ. Microbiol. 61, 3042-3050
69. Dervilly-Pinel, G., Thibault, J. F., and Saulnier, L. (2001) Experimental evidence for a semi-flexible conformation for arabinoxylans. Carbohydr. Res. 330, 365-372