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Plant Polysaccharide Xyloglucan and Enzymes That Hydrolyze It (Review)

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Abstract—

Various types of plant raw material are widely used in the pulp and paper, textile, food, and agricultural industries and pharmacology. One of the problems of utilizing the complex plant biomass is poor knowledge of its hemicellulose content and the lack of effective enzymes for hydrolysis of hemicelluloses. Xyloglucan is the major structural and storage polysaccharide in all dicots and a great number of monocots. It has a branched architecture with a backbone constructed of β-1,4-connected cellotetraose units decorated with short sidechains composed of xylose, galactose, arabinose, fucose and some other residues. Sidechain composition and alternation order are specie-specific and can change during cell growth resulting in variety of xyloglucan structural types. In general, xyloglucan structure depends on the taxonomic position of the plant. Structural features of xyloglucans belonging to different taxonomic groups are discussed in the evolutionary aspect. Xyloglucan hydrolysis is a necessary condition during conversion of plant biomass into high added-value products. Variety of xyloglucan structural types complicates the selection of enzymes for its hydrolysis. Xyloglucanase-containing multienzyme complexes can be used for efficient decomposition of plant biomass polysaccharides into fermentable sugars for biotechnology, and for the improvement of feed quality. Investigation of xyloglucanases is necessary for the development of methods for protecting plants from pathogenic microorganisms, which use these enzymes in the invasion of plant tissue. The article discusses structural features of xyloglucans from different taxonomic groups in the evolutionary aspect and reviews selection of xyloglucanases for efficient hydrolysis of complex plant biomass.

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REFERENCES

  1. Carpita, N.C., Defernez, M., Findlay, K., Wells, B., Shoue, D.A., Catchpole, G., Wilson, R.H., and McCann, M.C., Cell wall architecture of the elongating maize coleoptile, Plant. Physiol., 2001, vol. 127, no. 2, pp. 551–565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gorshkova, T.A., Rastitel’naya kletochnaya stenka kak dinamichnaya sistema (Plant Cell Wall as a Dynamic System), Moscow, 2007.

  3. Fry, S.C., Cross-linking of matrix polymers in the growing cell walls of angiosperms, Annu. Rev. Plant. Physiol., 1986, vol. 37, pp. 165–186.

    Article  CAS  Google Scholar 

  4. Bacic, A., Harris, P.J., and Stone, B.A., Structure and function of plant cell walls, in The Biochemistry of Plants: A Comprehensive Treatise, vol. 14: Carbohydrates, New York: Academic, 1988, pp. 297–371.

    Chapter  Google Scholar 

  5. Dudkin, M.S. and Gromov, V.S., Gemitsellyulozy (Hemicelluloses), Riga, 1991.

    Google Scholar 

  6. McNeil, M., Darvill, A.G., Fry, S.C., and Albersheim, P., Structure and function of the primary cell walls of plants, Annu. Rev. Biochem., 1984, vol. 53, pp. 625–663.

    Article  CAS  PubMed  Google Scholar 

  7. Fry, S.C., The structure and functions of xyloglucan, J. Exp. Bot., 1989, vol. 40, no. 210, pp. 1–11.

    Article  CAS  Google Scholar 

  8. Fry, S.C., Aldington, S., Hetherington, P.R., and Aitken, J., Oligosaccharides as signals and substrates in the plant cell wall, Plant Physiol., 1993, vol. 103, no. 1, pp. 1–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schultink, A., Liu, L., Zhu, L., and Pauly, M., Structural diversity and function of xyloglucan sidechain substituents, Plants, 2014, vol. 3, no. 4, pp. 526–542.

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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.G., Seitz, H.U., Selvendran, R.R., Voragen, A.G.J., and White, A.R., An unambiguous nomenclature for xyloglucan-derived oligosaccharides, Physiol. Plant., 1993, vol. 89, no. 1, pp. 1–3.

    Article  CAS  Google Scholar 

  11. Popper, Z.A. and Fry, S.C., Primary cell wall composition of bryophytes and charophytes, Ann. Bot., 2003, vol. 91, no. 1, pp. 1–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Popper, Z.A. and Fry, S.C., Primary cell wall composition of pteridophytes and spermatophytes, New Phytol., 2004, vol. 164, no. 1, pp. 165–174.

    Article  CAS  PubMed  Google Scholar 

  13. Vissenberg, K., Sandt, V.V., Fry, S.C., and Verbelen, J.-P., Xyloglucan endotransglucosylase action is high in the root elongation zone and in the trichoblasts of all vascular plants from Sellaginella to Zea mays,J. Exp. Bot., 2003, vol. 54, no. 381, pp. 335–344.

    Article  CAS  PubMed  Google Scholar 

  14. Peña, M.J., Darvill, A.G., Eberhard, S., York, W.S., and O’Neill, M.A., Moss and liverwort xyloglucans contain galacturonic acid and are structurally distinct from the xyloglucans synthesized by hornworts and vascular plants, Glycobiology, 2008, vol. 18, no. 11, pp. 891–904.

    Article  PubMed  CAS  Google Scholar 

  15. Hsieh, Y.S. and Harris, P.J., Structures of xyloglucans in primary cell walls of gymnosperms, monilophytes (ferns sensu lato) and lycophytes, Phytochemistry, 2012, vol. 79, pp. 87–101.

    Article  CAS  PubMed  Google Scholar 

  16. Kakegawa, K., Edashige, Y., and Ishii, T., Xyloglucan from xylem-differentiating zones of Cryptomeria japonica,Phytochemistry, 1998, vol. 47, no. 5, pp. 767–771.

    Article  CAS  PubMed  Google Scholar 

  17. Hoffman, M., Jia, Z., Pena, M.J., et al., Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae, Carbohydr. Res., 2005, vol. 340, no. 11, pp. 1826–1840.

    Article  CAS  PubMed  Google Scholar 

  18. Buckeridge, M.S., Seed cell wall storage polysaccharides: Models to understand cell wall biosynthesis and degradation, Plant Physiol., 2000, vol. 154, no. 3, pp. 1017–1023.

    Article  CAS  Google Scholar 

  19. Vinueza, N.R., Gallardo, V.A., Klimek, J.F., Carpita, N.C., Kenttamaa, H.I., et al., Analysis of xyloglucans by ambient chloride attachment ionization tandem mass spectrometry, Carbohydr. Res., 2013, vol. 98, no. 1, pp. 1203–1213.

    Article  CAS  Google Scholar 

  20. Aboughe-Angone, S., Nguema-Ona, E., Ghosh, P., Lerouge, P., Ishii, T., Ray, B., and Driouich, A., Cell wall carbohydrates from fruit pulp of Argania spinosa: Structural analysis of pectin and xyloglucan polysaccharides, Carbohydr. Res., 2008, vol. 343, no. 1, pp. 67–72.

    Article  CAS  PubMed  Google Scholar 

  21. Jia, Z., Cash, M., Darvill, A.G., and York, W.S., NMR characterization of endogenously o-acetylated oligosaccharides isolated from tomato (Lycopersicon esculentum) xyloglucan, Carbohydr. Res., 2005, vol. 340, no. 11, pp. 1818–1825.

    Article  CAS  PubMed  Google Scholar 

  22. Jia, Z., Qin, Q., Darvill, A.G., and York, W.S., Structure of the xyloglucan produced by suspension-cultured tomato cells, Carbohydr. Res., 2003, vol. 338, no. 11, pp. 1197–1208.

    Article  CAS  PubMed  Google Scholar 

  23. Assor, C., Quemener, B., Vigouroux, J., and Lahaye, M., Fractionation and structural characterization of LiCl–DMSO soluble hemicelluloses from tomato, Carbohydr. Res., 2013, vol. 94, no. 1, pp. 46–55.

    Article  CAS  Google Scholar 

  24. Galvez-Lopez, D.F. and Laurens, B., Variability of cell wall polysaccharides composition and hemicellulose enzymatic profile in an apple progeny, Int. J. Biol. Macromol., 2011, vol. 49, no. 5, pp. 1104–1109.

    Article  CAS  PubMed  Google Scholar 

  25. Ray, S., Vigouroux, J., Quemener, B., Bonnin, E., and Lahaye, M., Novel and diverse fine structures in LiCl–DMSO extracted apple hemicelluloses, Carbohydr. Res., 2014, vol. 108, pp. 46–57.

    Article  CAS  Google Scholar 

  26. Lahaye, M., Falourd, X., Quemener, B., Ralet, M.C., Howad, W., Dirlewanger, E., and Arus, P., Cell wall polysaccharide chemistry of peach genotypes with contrasted textures and other fruit traits, J. Agric. Food Chem., 2012, vol. 60, no. 26, pp. 6594–6605.

    Article  CAS  PubMed  Google Scholar 

  27. Lerouxel, O., Choo, T.S., Seveno, M., Usadel, B., Faye, L., Lerouge, P., and Pauly, M., Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting, Plant Physiol., 2002, vol. 130, no. 4, pp. 1754–1763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Louvet, R., Rayon, C., Domon, M.-J., Rusterucci, C., Fournet, F., Leaustic, A., Crépeau, M.J., Ralet, M.C., Rihouey, C., Bardor, M., Lerouge, P., Gillet, F., and Pelloux, J., Major changes in the cell wall during silique development in Arabidopsis thaliana,Phytochemistry, 2011, vol. 72, no. 1, pp. 59–67.

    Article  CAS  PubMed  Google Scholar 

  29. Peña, M.J., Kong, Y., York, W.S., and O’Neill, M.A., A galacturonic acid-containing xyloglucan is involved in Arabidopsis root hair tip growth, Plant Cell, 2012, vol. 24, no. 11, pp. 4511–4524.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Pustjens, A.M., Schols, H.A., Kabel, M.A., and Gruppen, H., Characterisation of cell wall polysaccharides from rapeseed (Brassica napus) meal, Carbohydr. Res., 2013, vol. 98, no. 2, pp. 1650–1656.

    Article  CAS  Google Scholar 

  31. Huisman, M., Weel, K., Schols, H., and Voragen, A.G.J., Xyloglucan from soybean (Glycine max) meal is composed of XXXG-type building units, Carbohydr. Res., 2000, vol. 42, no. 2, pp. 185–191.

    Article  CAS  Google Scholar 

  32. Alonso-Simón, A., Neumetzler, L., García-Angulo, P., Encina, A.E., Acebes, J.L., Álvarez, J.M., and Hayashi, T., Plasticity of xyloglucan composition in bean (Phaseolus vulgaris)-cultured cells during habituation and dehabituation to lethal concentrations of dichlobenil, Mol. Plant, 2010, vol. 3, no. 3, pp. 603–609.

    Article  PubMed  CAS  Google Scholar 

  33. Ren, Y., Picout, D.R., Ellis, P.R., Ross-Murphy, S.B., and Reid, J.S., A novel xyloglucan from seeds of Afzelia africana Se. Pers.—extraction, characterization, and conformational properties, Carbohydr. Res., 2005, vol. 340, no. 5, pp. 997–1005.

    Article  CAS  PubMed  Google Scholar 

  34. Pauly, M., Qin, Q., Greene, H., Albersheim, P., Darvill, A., and York, W.S., Changes in the structure of xyloglucan during cell elongation, Planta, 2001, vol. 212, nos. 5–6, pp. 842–850.

    Article  CAS  PubMed  Google Scholar 

  35. York, W.S., Oates, J.E., Van Halbeck, H., Darvill, A.G., Albersheim, P., Tiller, P.R., and Dell, A., Location of o-acetyl substituents on a nonasaccharide repeating unit of sycamore extracellular xyloglucan, Carbohydr. Res., 1988, vol. 173, no. 1, pp. 113–132.

    Article  CAS  PubMed  Google Scholar 

  36. Takhtadjan, A., Diversity and Classification of Flowering Plants, New York: Columbia Univ. Press, 1997.

    Google Scholar 

  37. Verma, D.P.S., Maclachlan, G.A., Byrne, H., and Ewings, D., Regulation and in vitro translation of messenger ribonucleic acid for cellulase from auxin-treated pea epicotyls, J. Biol. Chem., 1975, vol. 250, no. 3, pp. 1019–1026.

    CAS  PubMed  Google Scholar 

  38. Hayashi, T. and Maclachlan, G., Pea xyloglucan and cellulose. III. Metabolism during lateral expansion of pea epicotyl cells, Plant Physiol., 1984, vol. 76, no. 3, pp. 739–742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Planta, E.M., Dea, I.C.M., and Bulpin, P.V., Xyloglucan (amyloid) mobilization in the cotyledons of Tropaeolum majus L. seeds following germination, Planta, 1985, vol. 163, no. 1, pp. 133–140.

    Article  Google Scholar 

  40. Siddalinga, MurthyK.R. and Kantharaju, S., Studies on xyloglucanase during the germination of seeds of Tamarindus indica, J. Biosci.,Medicines, 2014, vol. 2, no. 4, pp. 36–43.

  41. Koyama, T., Hayashi, T., Kato, Y., and Matsuda, K., Degradation of xyloglucan by wall-bound enzymes from soybean tissue. ii. degradation of the fragment hepta-saccharide from xyloglucan and the characteristic action pattern of the α-D-xylosidase in the enzyme system, Plant Cell Physiol., 1983, vol. 24, no. 2, pp. 155–162.

    Article  CAS  Google Scholar 

  42. O’Neil, R.A., White, A.R., York, W.S., Darvill, A.G., and Albersheim, P., A gas chromatographic-mass spectrometric assay for glycosylases, Phytochemistry, 1988, vol. 27, no. 2, pp. 329–333.

    Article  Google Scholar 

  43. Fry, S.C., Smith, R.C., Renwick, K.F., Martin, D.J., Hodge, S.K., and Matthews, K.J., Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants, Biochemistry, 1992, vol. 282, pp. 821–828.

    Article  CAS  Google Scholar 

  44. Nishitani, K. and Tominaga, R., Endoxyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule, J. Biol. Chem., 1992, vol. 267, no. 29, pp. 21058–21064.

    CAS  PubMed  Google Scholar 

  45. Rose, J.K.C., Braam, J., Fry, S.C., and Nishitani, K., The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature, Plant Cell Physiol., 2002, vol. 43, no. 12, pp. 1421–1435.

    Article  CAS  PubMed  Google Scholar 

  46. Eklöf, J.M. and Brumer, H., The XTH gene family: An update on enzyme structure, function, and phylogeny in xyloglucan remodeling, Plant Physiol., 2010, vol. 153, no. 2, pp. 456–466.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Ito, H. and Nishitani, K., Visualization of EXGT-mediated molecular grafting activity by means of a fluorescent-labeled xyloglucan oligomer, Plant Cell Physiol., 1999, vol. 40, no. 11, pp. 1172–1176.

    Article  CAS  Google Scholar 

  48. Vissenberg, K., Martinez-Vilchez, I.M., Verbelen, J.-P., and Miller, J.G., In vivo colocalization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots, Plant Cell, 2000, vol. 12, no. 7, pp. 1229–1238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mellerowicz, E.J., Immerzeel, P., and Hayashi, T., Xyloglucan: the molecular muscle of trees, Ann. Bot., 2008, vol. 102, no. 2, pp. 659–665.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Thompson, J.E., Smith, R.C., and Fry, S.C., Xyloglucan undergoes interpolymeric transglycosylation during binding to the plant cell wall in vivo: Evidence from 13C/3H dual labeling and isopycnic centrifugation in caesium trifluoroacetate, Biochem. J., 1997, vol. 327, pp. 699–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Thompson, J.E. and Fry, S.C., Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells, Plant J., 2001, vol. 26, no. 1, pp. 23–34.

    Article  CAS  PubMed  Google Scholar 

  52. Maris, A., Suslov, D., Fry, S.C., and Verbelen, J.P., Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension, J. Exp. Bot., 2009, vol. 60, no. 13, pp. 3959–3972.

    Article  CAS  PubMed  Google Scholar 

  53. Sasidharan, R., Chinnappa, C.C., Staal, M., Elzenga, J.T., Yokoyama, R., Nishitani, K., Voesenek, L.A., and Pierik, R., Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by xyloglucan endotransglucosylase/hydrolases, Plant Physiol., 2010, vol. 154, no. 2, pp. 978–990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Harada, T., Torii, Y., Morita, S., et al., Cloning, characterization, and expression of xyloglucan endotransglucosylase/hydrolase and expansin genes associated with petal growth and development during carnation flower opening, J. Exp. Bot., 2011, vol. 62, no. 2, pp. 815–823.

    Article  CAS  PubMed  Google Scholar 

  55. Miedes, E., Zarra, I., Hoson, T., et al., Xyloglucan endotransglucosylase and cell wall extensibility, J. Plant Physiol., 2011, vol. 168, no. 3, pp. 196–203.

    Article  CAS  PubMed  Google Scholar 

  56. Frankova, L. and Fry, S.C., trans-α-Xylosidase and trans-β-galactosidase activities, widespread in plants, modify and stabilize xyloglucan structures, Plant J., 2012, vol. 71, no. 1, pp. 45–60.

    Article  CAS  PubMed  Google Scholar 

  57. Edwards, M., Dea, I.C.M., Bulpin, P.V., and Reid, J.S.G., Purification and properties of a nove1 xyloglucan-specific endo-1,4-beta-D-glucanase from germinated nasturtium seeds, J. Biol. Chem., 1986, vol. 261, no. 20, pp. 9489–9494.

    CAS  PubMed  Google Scholar 

  58. Fanutti, C., Gidley, M.J., and Reid, J.S.G., Action of a pure xyloglucan endo-transglycosylase (formerly called xyloglucan-specific endo-(1,4)-beta-D-glucanase from the cotyledons of germinated nasturtium seed, Plant J., 1993, vol. 3, no. 5, pp. 691–700.

    Article  CAS  PubMed  Google Scholar 

  59. Hanna, R., Brummell, D.A., Camirand, A., Hensel, A., Russell, E.F., and Maclachlan, G.A., Solubilization and properties of GDP-fucose:xyloglucan 1,2-alpha-L-fucosyltransferase from pea epicotyl membranes, Arch. Biochem. Biophys., 1991, vol. 290, no. 1, pp. 7–13.

    Article  CAS  PubMed  Google Scholar 

  60. Redgwel, R.J. and Fry, S.C., Xyloglucan endo-transglycosylase activity increases during kiwifruit (Actinidia deliciosa) ripening. (Implications for fruit softening), Plant. Physiol., 1993, vol. 103, no. 4, pp. 1399–1406.

    Article  Google Scholar 

  61. Lashbrook, C.C., Gonzalez-Bosch, C., and Bennet, A., Two divergent endo-beta-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers, Plant Cell, 1994, vol. 6, no. 10, pp. 1485–1493.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Gloster, T.M., Ibatullin, F.M., Macauley, K., Eklöf, J.M., Roberts, S., Turkenburg, J.P., Bjørnvad, M.E., Jørgensen, P.L., Danielsen, S., Johansen, K.S., Borchert, T.V., Wilson, K.S., Brumer, H., and Davies, G.J., Characterization and three-dimensional structures of two distinct bacterial xyloglucanases from families GH5 and GH12, J. Biol. Chem., 2007, vol. 282, no. 26, pp. 19177–19189.

    Article  CAS  PubMed  Google Scholar 

  63. Mark, P., Baumann, M.J., Eklöf, J.M., Gullfot, F., Michel, G., Kallas, A.M., Teeri, T.T., Brumer, H., and Czjzek, M., 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, 2009, vol. 75, no. 4, pp. 820–836.

    Article  CAS  PubMed  Google Scholar 

  64. Schnorr, K., Jørgensen, P.L., and Schulein, M., Family 44 xyloglucanases, US Patent no. 6815192, 2004.

  65. Martinez-Fleites, C., Guerreiro, C.I., Baumann, M.J., Taylor, E.J., Prates, J.A., Ferreira, L.M., Fontes, C.M., Brumer, H., and Davies, G.J., Crystal structures of Clostridium thermocellum xyloglucanase, XGH74A, reveal the structural basis for xyloglucan recognition and degradation, J. Biol. Chem., 2006, vol. 281, no. 34, pp. 24922–24933.

    Article  CAS  PubMed  Google Scholar 

  66. Yaoi, K., Kondo, H., Noro, N., Suzuki, M., Tsuda, S., and Mitsuishi, Y., Tandem repeat of a seven-bladed beta-propeller domain in oligoxyloglucan reducing-end-specific cellobiohydrolase, Structure, 2004, vol. 12, no. 7, pp. 1209–1217.

    Article  CAS  PubMed  Google Scholar 

  67. Sulzenbacher, G., Divne, C., Jones, T.A., Wöldike, H.F., Schülein, M., Withers, S.G., and Davies, G.J., Crystal structure of the family 7 endoglucanase I (Cel7B) from Humicola insolens at 2.2 Å resolution and identification of the catalytic nucleophile by trapping of the covalent glycosyl-enzyme intermediate, Biochem. J., 1998, vol. 335, pp. 409–416.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Chhabra, S.R. and Kelly, R.M., Biochemical characterization of Thermotoga maritima endoglucanase cel74 with and without a carbohydrate binding module (CBM), FEBS Lett., 2002, vol. 531, no. 2, pp. 375–380.

    Article  CAS  PubMed  Google Scholar 

  69. Larner, J., Other glucosidases, in The Enzymes, New York: Academic, 1960, vol. 4, pp. 369–378.

    Google Scholar 

  70. Yao, K. and Mitsuishi, Y., Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase, J. Biol. Chem., 2002, vol. 277, no. 50, pp. 48276–48281.

    Article  Google Scholar 

  71. Pauly, M., Andersen, L.N., Kaupinnen, S., Kofod, L.V., York, W.S., Albersheim, P., and Darvill, A., A xyloglucan specific endo-β-1,4-glucanase from Aspergillus aculeatus: Expression cloning in yeast, purification and characterization of the recombinant enzyme, Glycobiology, 1999, vol. 9, no. 1, pp. 93–100.

    Article  CAS  PubMed  Google Scholar 

  72. Rabinovich, M.L., Melnick, M.S., and Bolobova, A.V., The structure and mechanism of action of cellulolytic enzymes, Biochemistry (Moscow), 2002, vol. 67, no. 8, pp. 850–571.

    CAS  PubMed  Google Scholar 

  73. Davies, G. and Henrissat, B., Structures and mechanisms of glycosyl hydrolases, Structure, 1995, vol. 3, no. 9, pp. 853–859.

    Article  CAS  PubMed  Google Scholar 

  74. McCarte, J.D. and Withers, S.G., Mechanisms of enzymatic glycoside hydrolysis, Curr. Opin. Struct. Biol., 1994, vol. 4, no. 6, pp. 885–892.

    Article  Google Scholar 

  75. Henrissat, B. and Davies, G., Structural and sequence-based classification of glycoside hydrolases, Curr. Opin. Struct. Biol., 1997, vol. 7, no. 5, pp. 637–644.

    Article  CAS  PubMed  Google Scholar 

  76. Vasella, A., Davies, G.J., and Bohm, M., Glycosidase mechanisms, Curr. Opin. Chem. Biol., 2002, vol. 6, no. 5, pp. 619–629.

    Article  CAS  PubMed  Google Scholar 

  77. Henrissat, B. and Bairoch, A., New families in the classification of glycosyl hydrolases based on amino-acid sequence similarities, Biochem. J., 1993, vol. 293, pp. 781–788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Gebler, J., Gilkes, N.R., Claeyssens, M., Wilson, D.B., Beguin, P., Wakarchuk, W.W., Kilburn, D.G., Miller, R.C., Jr., Warren, R.A., and Withers, S.G., Stereoselective hydrolysis catalyzed by related beta-1,4-glucanases and beta-1,4-xylanases, J. Biol.Chem., 1992, vol. 267, no. 18, pp. 12559–12561.

    CAS  PubMed  Google Scholar 

  79. Gloster, T.M., Turkenburg, J.P., Potts, J.R., Henrissat, B., and Davies, G.J., Divergence of catalytic mechanism within a glycosidase family provides insight into evolution of carbohydrate metabolism by human gut flora, Chem. Biol., 2008, vol. 15, no. 10, pp. 1058–1067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Rye, C.S. and Withers, S.G., Glycosidase mechanisms, Curr. Opin. Chem. Biol., 2000, vol. 4, no. 5, pp. 573–580.

    Article  CAS  PubMed  Google Scholar 

  81. Thompson, J., Ruvinov, S.B., Freedberg, D.I., and Hall, B.G., Cellobiose-6-phosphate hydrolase (CelF) of Escherichia coli: Characterization and assignment to the unusual family 4 of glycosylhydrolases, J. Bacteriol., 1999, vol. 181, no. 23, pp. 7339–7345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Ichinose, H., Araki, Y., Michikawa, M., Harazono, K., Yaoi, K., Karita, S., and Kaneko, S., Characterization of an endo-processive-type xyloglucanase having a β‑1,4-glucan-binding module and an endo-type xyloglucanase from Streptomyces avermitiles,Appl. Environ. Microbiol., 2012, vol. 78, no. 22, pp. 7939–7945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Qi, H., Bai, F., and Liu, A., Purification and characteristics of xyloglucanase and five other cellulolytic enzymes from Trichoderma reesei QM9414, Biochemistry (Moscow), 2013, vol. 78, no. 4, pp. 548–555.

    Google Scholar 

  84. Grishutin, S.G., Gusakov, A.V., Markov, A.V., Ustinov, B.B., Semenova, M.V., and Sinitsyn, A.P., Specific xyloglucanases as a new class of polysaccharide-degrading enzymes, Biochim. Biophys. Acta, 2004, vol. 1674, pp. 268–281.

    Article  CAS  PubMed  Google Scholar 

  85. Yaoi, K. and Mitsuishi, Y., Purification, characterization, cDNA cloning, and expression of a xyloglucan endoglucanase from Geotrichum sp. M128, FEBS Lett., 2004, vol. 560, pp. 45–50.

    Article  CAS  PubMed  Google Scholar 

  86. Yaoi, K. and Mitsuishi, Y., Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase, J. Biol. Chem., 2002, vol. 277, no. 50, pp. 48276–48281.

    Article  CAS  PubMed  Google Scholar 

  87. Master, E.R., Zheng, Y., Storms, R., Tsang, A., and Powlowski, J., A xyloglucan-specific family 12 glycosyl hydrolase from Aspergillus niger: Recombinant expression, purification and characterization, Biochem. J., 2008, vol. 411, no. 1, pp. 161–170.

    Article  CAS  PubMed  Google Scholar 

  88. Hasper, A., Dekkers, E., van Mill, M., van de Vondervoort, P.J., and de Graaff, L.H., EglC, a new endoglucanase from Aspergillius niger with major activity towards xyloglucan, Appl. Environ. Microbiol., 2002, vol. 68, no. 4, pp. 1556–1560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Takada, G., Kawasaki, M., Kitawaki, M., Kawaguchi, T., Sumitani, J., Izumori, K., and Arai, M., Cloning and transcription analysis of the Aspergillus aculeatus No. F-50 endoglucanase 2 (cmc2) gene, J. Biosci. Bioeng., 2002, vol. 94, no. 5, pp. 482–485.

    Article  CAS  PubMed  Google Scholar 

  90. Damasio, A.R.L., Pessela, B.C., Mateo, C., Segato, F., Prade, R.A., Guisan, J.M., and Polizeli, M.L.T.M., Immobilization of a recombinant endo-15-arabinanase secreted by Aspergillus nidulans strain A773, J. Mol. Catal., 2012, vol. 77, pp. 39–45.

    CAS  Google Scholar 

  91. Markov, A.V., Gusakov, A.V., Kondratyeva, E.G., Okunev, O.N., Bekkarevich, A.O., and Sinitsyn, A.P., New effective method for analysis of the component composition of enzyme complexes from Trichoderma reesei,Biochemistry, 2005, vol. 70, no. 6, 657–663.

    CAS  PubMed  Google Scholar 

  92. Rey, M., Zaretsky, E., and Haas, J., Polypeptides having xyloglucanase activity and nucleic acids encoding same, US Patent no. 20040067569A1, 2004.

  93. Ishida, T., Yaoi, K., Hiyoshi, A., Igarashi, K., and Samejima, M., Substrate recognition by glycoside hydrolase family 74 xyloglucanase from the basidiomycete Phanerochaete chrysosporium,FEBS J., 2007, vol. 274, no. 21, pp. 5727–5736.

    Article  CAS  PubMed  Google Scholar 

  94. Sinitsyna, O.A., Fedorova, E.A., Pravilnikov, A.G., Rozhkova, A.M., Skomarovsky, A.A., Matys, V.Y., Bubnova, T.M., Okunev, O.N., Vinetsky, Y.P., and Sinitsyn, A.P., Isolation and properties of xyloglucanases of Penicillium sp., Biochemistry, 2010, vol. 75, no. 1, pp. 41–49.

    CAS  PubMed  Google Scholar 

  95. Vinetskii, Yu.P., Okunev, O.N., Sinitsyn, A.P., Sinitsyna, O.A., Sokolova, L.M., Fedorova, E.A., and Chernoglazov, V.M., A method for obtaining an enzyme preparation hydrolyze hemicellulosic heteropolysaccharides of plant cell wall and the enzyme preparation (variants), RF Patent no. 2358756, 2009.

  96. Habrylo, O., Song, X., Forster, A., Jeltsch, J.M., and Phalip, V., Characterization of the four GH12 endoxylanases from the plant pathogen Fusarium graminearum,J. Microbiol Biotechnol., 2012, vol. 22, no. 8, pp. 1118–1126.

    Article  CAS  PubMed  Google Scholar 

  97. Song, S., Tang, Y., Yang, S., Yan, Q., Zhou, P., and Jiang, Z., Characterization of two novel family 12 xyloglucanases from the thermophilic Rhizomucor miehei,Appl. Microbiol. Biotechnol., 2013, vol. 97, no. 23, pp. 10013–10024.

    Article  CAS  PubMed  Google Scholar 

  98. Vlasenko, E.Y., Ding, H., Labavitch, J.M., and Shoemaker, S.P., Enzymatic hydrolysis of pretreated rice straw, Biores. Technol., 1997, vol. 59, pp. 109–119.

    Article  CAS  Google Scholar 

  99. Baker, J.O., Adney, W.S., Nleves, R.A., Thomas, S., Wilson, D., and Himmel, M.E., A new thermostable endoglucanase, Acidothermus cellulolyticus E1: Synergism with Trichoderma reesei CBH I and comparison to Thermomonospora fusca E5, Appl. Biochem. Biotechnol., 1994, vol. 45, no. 1, pp. 245–256.

    Article  Google Scholar 

  100. Biswas, G.C.G., Ransom, C., and Sticklen, M., Expression of biologically active Acidothermus cellulolyticus endoglucanase in transgenic maize plants, Plant Sci., 2006, vol. 171, no. 5, pp. 617–623.

    Article  CAS  Google Scholar 

  101. Takeda, T., Nakano, Y., Takahashi, M., Sakamoto, Y., and Konno, N., Polysaccharide-inducible endoglucanases from Lentinula edodes exhibit a preferential hydrolysis of 1,3–1,4-β-glucan and xyloglucan, Agric. Food Chem., 2013, vol. 61, no. 31, pp. 7591–7598.

    Article  CAS  Google Scholar 

  102. Tsang, A, Powlowski, J., and Butler, G., Novel cell wall deconstruction enzymes of Malbranchea cinnamomea, Thielavia australiensis, and Paecilomyces byssochlamydoides, and uses thereof, WO Patent no. 2014138983A1, 2014.

  103. Tsang, A, Powlowski, J., and Butler, G., Novel cell wall deconstruction enzymes of Amorphotheca resinae, Rhizomucor pusillus, and Calcarisporiella thermophila, and uses thereof, WO Patent no. 2014110675A1, 2014.

  104. Wu, W., Schulein, M., Kauppinen, M.S., and Stringer, M.A., Xyloglucanase from Malbranchea, US Patent no. 6500658, 2002.

  105. Tsang, A., Powlowski, J., Butler, G., and Storm, R., Novel cell wall deconstruction enzymes and uses thereof, WO Patent no. 2012092676, 2012.

  106. Sinitsyn, A.P., Okunev, O.N., Chernoglazov, V.M., Sinitsyna, O.A., and Popov, V.O., The filamentous fungus Penicillium verruculosum strain producing a complex of cellulases, xylanases, and xyloglucanases and the method of producing the enzyme preparation containing the complex of cellulases, xylanases, and xyloglucanases for the hydrolysis of cellulose and hemicellulose, RF Patent no. 2361918, 2009.

  107. Okunev, O.N., Skomarovskii, A.A., Zorov, I.N., Sinitsyn, A.P., Popov, V.O., and Chernoglazov, V.M., The filamentous fungus Penicillium funiculosum strain producing a carbohydrase complex containing cellulase, beta-glucanase, beta-glucosidase, xylanase, and xyloglucanase and a method for producing an enzyme preparation carbohydrase complex for saccharification of lignocellulosic materials, RF Patent no. 2323254, 2008.

  108. Okunev, O.N., Sinitsyn, A.P., and Chernoglazov, V.M., The filamentous fungus Aspergillus aculeatus strain producing carbohydrase complex containing xylanases, beta-glucanases, pectinases, and xyloglucanases, RF Patent no. 2303057, 2007.

  109. Krestyanova, I.N., Sakhibgaraeva, L.F., Berezina, O.V., Rykov, S.V., Zavyalov, A.V., Zverlov, V.V., and Yarotsky, S.V., Characteristics of fungal strains producing thermostable xyloglucanases from the Russian National Collection of industrial microorganisms, Mol. Gen. Microbiol. Virol., 2016, vol. 31, no. 3, pp. 149–155.

    Article  Google Scholar 

  110. Berezina, O.V., Herlet, J., Rykov, S.V., Kornberger, P., Zavyalov, A., Kozlov, D., Sakhibgaraeva, L., Krestyanova, I., Schwarz, W.H., Zverlov, V.V., Liebl, W., and Yarotsky, S.V., Thermostable multifunctional GH74 xyloglucanase from Myceliophthora thermophila: high-level expression in Pichia pastoris and characterization of the recombinant protein, Appl. Microbiol. Biotechnol., 2017, vol. 101, no. 14, pp. 5653–5666.

    Article  CAS  PubMed  Google Scholar 

  111. Zverlov, V.V., Schantz, N., Schmitt-Kopplin, P., and Schwarz, W.H., Two new major subunits in the cellulosome of Clostridium thermocellum: Xyloglucanase Xgh74A and endoxylanase Xyn10D, Microbiology, 2005, vol. 151, pp. 3395–3401.

    Article  CAS  PubMed  Google Scholar 

  112. Ravachol, J., de Philip, P., Borne, R., et al., Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum,Sci. Rep., 2016, vol. 6, p. 22770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Sinitsyn, A.P., Properties of enzyme complexes, used as feed additives, in 23-i Nauchno-prakticheskii seminar po optimizatsii kormleniya sel’skokhozyaystvennykh zhivotnykh. OOO “Agroferment,” 23 oktyabrya 2015 (23rd Scientific and Practical Workshop on Optimization of Feeding of Farm Animals, LLC Agroferment, October 23, 2015). http://agroferment.ru/images/ferm2.pdf.

  114. Heimbach, J., Determination of the GRAS Status of the Addition of Tamarind Seed Polysaccharide to Conventional Foods as a Stabilizer and Thickener, Prepared for DSP GOKYO FOOD & CHEMICAL Co., Ltd. Osaka, Japan, 2014.

    Google Scholar 

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ACKNOWLEDGMENTS

We thank Mariya Kharina, the Associate Professor at the Chemical Cybernetics Chair in Kazan National Research Technological University, for valuable advices and recommendations during writing the review.

Funding

This work was supported by the Ministry of Education and Science of the Russian Federation as a part of the Federal Target Program on Research and Development of Priority Lines in the Scientific and Technological Complex of Russia for 2014–2020; Subsidy Granting Agreement no. 14.628.21.0001; unique ID number of the agreement is RFMEF162814X0001.

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Authors and Affiliations

  1. Kurchatov Institute, National Research Center, State Research Institute of Genetics and Selection of Industrial Microorganisms, 117545, Moscow, Russia

    A. V. Zavyalov, S. V. Rykov, V. I. Sushkova, S. V. Yarotsky & O. V. Berezina

  2. Institute of Molecular Genetics, Russian Academy of Sciences, 123182, Moscow, Russia

    N. A. Lunina

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  1. A. V. Zavyalov
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  2. S. V. Rykov
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  3. N. A. Lunina
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  4. V. I. Sushkova
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  5. S. V. Yarotsky
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  6. O. V. Berezina
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Correspondence to O. V. Berezina.

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Translated by E. Kuznetsova

Corresponding author: e-mail: mashchenko@yandex.ru.

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Zavyalov, A.V., Rykov, S.V., Lunina, N.A. et al. Plant Polysaccharide Xyloglucan and Enzymes That Hydrolyze It (Review). Russ J Bioorg Chem 45, 845–859 (2019). https://doi.org/10.1134/S1068162019070148

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