Insights into the mechanism(s) of digestion of crystalline cellulose by plant class C GH9 endoglucanases

  • Siddhartha KunduEmail author
Original Paper


Biofuels such as γ-valerolactone, bioethanol, and biodiesel are derived from potentially fermentable cellulose and vegetable oils. Plant class C GH9 endoglucanases are CBM49-encompassing hydrolases that cleave the β (1 → 4) glycosidic linkage of contiguous D-glucopyranose residues of crystalline cellulose. Here, I analyse 3D-homology models of characterised and putative class C enzymes to glean insights into the contribution of the GH9, linker, and CBM49 to the mechanism(s) of crystalline cellulose digestion. Crystalline cellulose may be accommodated in a surface groove which is imperfectly bounded by the GH9_CBM49, GH9_linker, and linker_CBM49 surfaces and thence digested in a solvent accessible subsurface cavity. The physical dimensions and distortions thereof, of the groove, are mediated in part by the bulky side chains of aromatic amino acids that comprise it and may also result in a strained geometry of the bound cellulose polymer. These data along with an almost complete absence of measurable cavities, along with poorly conserved, hydrophobic, and heterogeneous amino acid composition, increased atomic motion of the CBM49_linker junction, and docking experiements with ligands of lower degrees of polymerization suggests a modulatory rather than direct role for CBM49 in catalysis. Crystalline cellulose is the de facto substrate for CBM-containing plant and non-plant GH9 enzymes, a finding supported by exceptional sequence- and structural-homology. However, despite the implied similarity in general acid-base catalysis of crystalline cellulose, this study also highlights qualitative differences in substrate binding and glycosidic bond cleavage amongst class C members. Results presented may aid the development of novel plant-based GH9 endoglucanases that could extract and utilise potential fermentable carbohydrates from biomass.

Graphical Abstract

Crystalline cellulose digestion by plant class C GH9 endoglucanases - an in silico assessment of function.


Active-site geometry Carbohydrate binding module Class C GH9 endoglucanases Crystalline cellulose Glycoside hydrolase Homology modelling Interaction surface 



Amino acids


Carbohydrate binding module


Degree of polymerization


Enzyme commission


Full length


Glycoside hydrolase


Interaction surface




Normal mode analysis





SK wishes to formally thank Dr. Rita Sharma for her suggestions and unflinching moral support.

Author contribution

SK collated the data, conducted the analysis, developed the scoring indices, wrote all the necessary code, and the manuscript.

Supplementary material

894_2019_4133_MOESM1_ESM.pdf (21 kb)
ESM 1 (PDF 20 kb)
894_2019_4133_MOESM2_ESM.pdf (1.8 mb)
ESM 2 (PDF 1857 kb)
894_2019_4133_MOESM3_ESM.pdf (2.3 mb)
ESM 3 (PDF 2382 kb)
894_2019_4133_MOESM4_ESM.pdf (277 kb)
ESM 4 (PDF 276 kb)
894_2019_4133_MOESM5_ESM.pdf (209 kb)
ESM 5 (PDF 208 kb)
894_2019_4133_MOESM6_ESM.pdf (216 kb)
ESM 6 (PDF 215 kb)
894_2019_4133_MOESM7_ESM.pdf (283 kb)
ESM 7 (PDF 282 kb)
894_2019_4133_MOESM8_ESM.pdf (2.2 mb)
ESM 8 (PDF 2217 kb)
894_2019_4133_MOESM9_ESM.pdf (124 kb)
ESM 9 (PDF 123 kb)
894_2019_4133_MOESM10_ESM.pdf (156 kb)
ESM 10 (PDF 155 kb)
894_2019_4133_MOESM11_ESM.pdf (129 kb)
ESM 11 (PDF 129 kb)


  1. 1.
    Klemm D, Heublein B, Fink HP, Bohn A (2005) Cellulose: fascinating biopolymer and sustainable raw material. Angew Chem Int Ed Eng 44(22):3358–3393Google Scholar
  2. 2.
    Augimeri RV, Varley AJ, Strap JL (2015) Establishing a role for bacterial cellulose in environmental interactions: lessons learned from diverse biofilm-producing proteobacteria. Front Microbiol 6:1282PubMedPubMedCentralGoogle Scholar
  3. 3.
    Reardon-Robinson ME, Wu C, Mishra A, Chang C, Bier N, Das A, Ton-That H (2014) Pilus hijacking by a bacterial coaggregation factor critical for oral biofilm development. Proc Natl Acad Sci U S A 111(10):3835–3840PubMedPubMedCentralGoogle Scholar
  4. 4.
    Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32(3):420–424PubMedGoogle Scholar
  5. 5.
    Yoshida Y, Palmer RJ, Yang J, Kolenbrander PE, Cisar JO (2006) Streptococcal receptor polysaccharides: recognition molecules for oral biofilm formation. BMC Oral Health 6(Suppl 1):S12PubMedPubMedCentralGoogle Scholar
  6. 6.
    Agarwal V, Dauenhauer PJ, Huber GW, Auerbach SM (2012) Ab initio dynamics of cellulose pyrolysis: nascent decomposition pathways at 327 and 600 degrees C. J Am Chem Soc 134(36):14958–14972PubMedGoogle Scholar
  7. 7.
    Paulsen AD, Hough BR, Williams CL, Teixeira AR, Schwartz DT, Pfaendtner J, Dauenhauer PJ (2014) Fast pyrolysis of wood for biofuels: spatiotemporally resolved diffuse reflectance in situ spectroscopy of particles. ChemSusChemGoogle Scholar
  8. 8.
    Kundu S, Sharma R (2018) Origin, evolution, and divergence of plant class C GH9 endoglucanases. BMC Evol Biol 18:79PubMedPubMedCentralGoogle Scholar
  9. 9.
    del Campillo E, Gaddam S, Mettle-Amuah D, Heneks J (2012) A tale of two tissues: AtGH9C1 is an endo-beta-1,4-glucanase involved in root hair and endosperm development in Arabidopsis. PLoS One 7(11):e49363PubMedPubMedCentralGoogle Scholar
  10. 10.
    Kundu S (2015) Co-operative intermolecular kinetics of 2-oxoglutarate dependent dioxygenases may be essential for system-level regulation of plant cell physiology. Front Plant Sci 6:489PubMedPubMedCentralGoogle Scholar
  11. 11.
    Tan TC, Kracher D, Gandini R, Sygmund C, Kittl R, Haltrich D, Hallberg BM, Ludwig R, Divne C (2015) Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. Nat Commun 6:7542PubMedPubMedCentralGoogle Scholar
  12. 12.
    Westermark U, Eriksson K-E, Daasvatn K, Liaaen-Jensen S, Enzell CR, Mannervik B (1974) Cellobiose:quinone oxidoreductase, a new wood-degrading enzyme from white-rot fungi. Acta Chem Scand 28b:209–214Google Scholar
  13. 13.
    Schimz KL, Broll B, John B (1983) Cellobiose phosphorylase (EC of cellulomonas: occurrence, induction, and its role in cellobiose metabolism. Arch Microbiol 135(4):241–249Google Scholar
  14. 14.
    Sheth K, Alexander JK (1969) Purification and properties of beta-1,4-oligoglucan:orthophosphate glucosyltransferase from Clostridium thermocellum. J Biol Chem 244(2):457–464PubMedGoogle Scholar
  15. 15.
    Ye X, Zhu Z, Zhang C, Zhang YH (2011) Fusion of a family 9 cellulose-binding module improves catalytic potential of Clostridium thermocellum cellodextrin phosphorylase on insoluble cellulose. Appl Microbiol Biotechnol 92(3):551–560PubMedGoogle Scholar
  16. 16.
    Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42(Database issue):D490–D495PubMedGoogle Scholar
  17. 17.
    Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22:1273–1284PubMedGoogle Scholar
  18. 18.
    Kundu S, Sharma R (2016) In silico identification and taxonomic distribution of plant class C GH9 endoglucanases. Front Plant Sci 7:1185PubMedPubMedCentralGoogle Scholar
  19. 19.
    Ficko-Blean E, Boraston AB (2006) The interaction of a carbohydrate-binding module from a Clostridium perfringens N-acetyl-beta-hexosaminidase with its carbohydrate receptor. J Biol Chem 281(49):37748–37757PubMedGoogle Scholar
  20. 20.
    Duan CJ, Feng YL, Cao QL, Huang MY, Feng JX (2016) Identification of a novel family of carbohydrate-binding modules with broad ligand specificity. Sci Rep 6:19392PubMedPubMedCentralGoogle Scholar
  21. 21.
    Prates ET, Stankovic I, Silveira RL, Liberato MV, Henrique-Silva F, Pereira Jr N, Polikarpov I, Skaf MS (2013) X-ray structure and molecular dynamics simulations of endoglucanase 3 from Trichoderma harzianum: structural organization and substrate recognition by endoglucanases that lack cellulose binding module. PLoS One 8(3):e59069PubMedPubMedCentralGoogle Scholar
  22. 22.
    Boraston AB, Nurizzo D, Notenboom V, Ducros V, Rose DR, Kilburn DG, Davies GJ (2002) Differential oligosaccharide recognition by evolutionarily-related beta-1,4 and beta-1,3 glucan-binding modules. J Mol Biol 319(5):1143–1156PubMedGoogle Scholar
  23. 23.
    Charnock SJ, Bolam DN, Nurizzo D, Szabo L, McKie VA, Gilbert HJ, Davies GJ (2002) Promiscuity in ligand-binding: the three-dimensional structure of a Piromyces carbohydrate-binding module, CBM29-2, in complex with cello- and mannohexaose. Proc Natl Acad Sci U S A 99(22):14077–14082PubMedPubMedCentralGoogle Scholar
  24. 24.
    Crennell SJ, Cook D, Minns A, Svergun D, Andersen RL, Nordberg Karlsson E (2006) Dimerisation and an increase in active site aromatic groups as adaptations to high temperatures: X-ray solution scattering and substrate-bound crystal structures of Rhodothermus marinus endoglucanase Cel12A. J Mol Biol 356(1):57–71PubMedGoogle Scholar
  25. 25.
    Kim SJ, Kim SH, Shin SK, Hyeon JE, Han SO (2016) Mutation of a conserved tryptophan residue in the CBM3c of a GH9 endoglucanase inhibits activity. Int J Biol Macromol 92:159–166PubMedGoogle Scholar
  26. 26.
    Mattinen ML, Kontteli M, Kerovuo J, Linder M, Annila A, Lindeberg G, Reinikainen T, Drakenberg T (1997) Three-dimensional structures of three engineered cellulose-binding domains of cellobiohydrolase I from Trichoderma reesei. Protein Sci 6(2):294–303PubMedPubMedCentralGoogle Scholar
  27. 27.
    Morrill J, Kulcinskaja E, Sulewska AM, Lahtinen S, Stalbrand H, Svensson B, Abou Hachem M (2015) The GH5 1,4-beta-mannanase from Bifidobacterium animalis subsp. lactis Bl-04 possesses a low-affinity mannan-binding module and highlights the diversity of mannanolytic enzymes. BMC Biochem 16:26PubMedPubMedCentralGoogle Scholar
  28. 28.
    Nishijima H, Nozaki K, Mizuno M, Arai T, Amano Y (2015) Extra tyrosine in the carbohydrate-binding module of Irpex lacteus Xyn10B enhances its cellulose-binding ability. Biosci Biotechnol Biochem 79(5):738–746PubMedGoogle Scholar
  29. 29.
    Parsiegla G, Reverbel-Leroy C, Tardif C, Belaich JP, Driguez H, Haser R (2000) Crystal structures of the cellulase Cel48F in complex with inhibitors and substrates give insights into its processive action. Biochemistry 39(37):11238–11246PubMedGoogle Scholar
  30. 30.
    Simpson HD, Barras F (1999) Functional analysis of the carbohydrate-binding domains of Erwinia chrysanthemi Cel5 (endoglucanase Z) and an Escherichia coli putative chitinase. J Bacteriol 181(15):4611–4616PubMedPubMedCentralGoogle Scholar
  31. 31.
    Simpson PJ, Xie H, Bolam DN, Gilbert HJ, Williamson MP (2000) The structural basis for the ligand specificity of family 2 carbohydrate-binding modules. J Biol Chem 275(52):41137–41142PubMedGoogle Scholar
  32. 32.
    Strobel KL, Pfeiffer KA, Blanch HW, Clark DS (2015) Structural insights into the affinity of Cel7A carbohydrate-binding module for lignin. J Biol Chem 290(37):22818–22826PubMedPubMedCentralGoogle Scholar
  33. 33.
    Taylor CB, Talib MF, McCabe C, Bu L, Adney WS, Himmel ME, Crowley MF, Beckham GT (2012) Computational investigation of glycosylation effects on a family 1 carbohydrate-binding module. J Biol Chem 287(5):3147–3155PubMedGoogle Scholar
  34. 34.
    Yaniv O, Petkun S, Shimon LJ, Bayer EA, Lamed R, Frolow F (2012) A single mutation reforms the binding activity of an adhesion-deficient family 3 carbohydrate-binding module. Acta Crystallogr D Biol Crystallogr 68(Pt 7):819–828PubMedGoogle Scholar
  35. 35.
    Abbott DW, Hrynuik S, Boraston AB (2007) Identification and characterization of a novel periplasmic polygalacturonic acid binding protein from Yersinia enterolitica. J Mol Biol 367(4):1023–1033PubMedGoogle Scholar
  36. 36.
    Abramyan J, Stajich JE (2012) Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis. MBio 3(3):e00150–e00112PubMedPubMedCentralGoogle Scholar
  37. 37.
    Bachman ES, McClay DR (1996) Molecular cloning of the first metazoan beta-1,3 glucanase from eggs of the sea urchin Strongylocentrotus purpuratus. Proc Natl Acad Sci U S A 93(13):6808–6813PubMedPubMedCentralGoogle Scholar
  38. 38.
    Janecek S, Svensson B, MacGregor EA (2011) Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzym Microb Technol 49(5):429–440Google Scholar
  39. 39.
    Li S, Yang X, Bao M, Wu Y, Yu W, Han F (2015) Family 13 carbohydrate-binding module of alginate lyase from Agarivorans sp. L11 enhances its catalytic efficiency and thermostability, and alters its substrate preference and product distribution. FEMS Microbiol Lett:362(10)Google Scholar
  40. 40.
    Newstead SL, Watson JN, Bennet AJ, Taylor G (2005) Galactose recognition by the carbohydrate-binding module of a bacterial sialidase. Acta Crystallogr D Biol Crystallogr 61(Pt 11):1483–1491PubMedGoogle Scholar
  41. 41.
    Palomo M, Kralj S, van der Maarel MJ, Dijkhuizen L (2009) The unique branching patterns of Deinococcus glycogen branching enzymes are determined by their N-terminal domains. Appl Environ Microbiol 75(5):1355–1362PubMedPubMedCentralGoogle Scholar
  42. 42.
    Libertini E, Li Y, McQueen-Mason SJ (2004) Phylogenetic analysis of the plant endo-beta-1,4-glucanase gene family. J Mol Evol 58(5):506–515PubMedGoogle Scholar
  43. 43.
    Molhoj M, Pagant S, Hofte H (2002) Towards understanding the role of membrane-bound endo-beta-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol 43(12):1399–1406PubMedGoogle Scholar
  44. 44.
    Urbanowicz BR, Bennett AB, Del Campillo E, Catala C, Hayashi T, Henrissat B, Hofte H, McQueen-Mason SJ, Patterson SE, Shoseyov O et al (2007) Structural organization and a standardized nomenclature for plant endo-1,4-beta-glucanases (cellulases) of glycosyl hydrolase family 9. Plant Physiol 144(4):1693–1696PubMedPubMedCentralGoogle Scholar
  45. 45.
    Flint J, Bolam DN, Nurizzo D, Taylor EJ, Williamson MP, Walters C, Davies GJ, Gilbert HJ (2005) Probing the mechanism of ligand recognition in family 29 carbohydrate-binding modules. J Biol Chem 280(25):23718–23726PubMedGoogle Scholar
  46. 46.
    Montanier C, Flint JE, Bolam DN, Xie H, Liu Z, Rogowski A, Weiner DP, Ratnaparkhe S, Nurizzo D, Roberts SM et al (2010) Circular permutation provides an evolutionary link between two families of calcium-dependent carbohydrate binding modules. J Biol Chem 285(41):31742–31754PubMedPubMedCentralGoogle Scholar
  47. 47.
    Roske Y, Sunna A, Pfeil W, Heinemann U (2004) High-resolution crystal structures of Caldicellulosiruptor strain Rt8B.4 carbohydrate-binding module CBM27-1 and its complex with mannohexaose. J Mol Biol 340(3):543–554PubMedGoogle Scholar
  48. 48.
    Zhang C, Zhang W, Lu X (2015) Expression and characteristics of a Ca(2)(+)-dependent endoglucanase from Cytophaga hutchinsonii. Appl Microbiol Biotechnol 99(22):9617–9623PubMedGoogle Scholar
  49. 49.
    Tunnicliffe RB, Bolam DN, Pell G, Gilbert HJ, Williamson MP (2005) Structure of a mannan-specific family 35 carbohydrate-binding module: evidence for significant conformational changes upon ligand binding. J Mol Biol 347:287–296PubMedGoogle Scholar
  50. 50.
    Uni F, Lee S, Yatsunami R, Fukui T, Nakamura S (2009) Role of exposed aromatic residues in substrate-binding of CBM family 5 chitin-binding domain of alkaline chitinase. Nucleic Acids Symp Ser (Oxf) 53:311–312Google Scholar
  51. 51.
    Divne C, Ståhlberg J, Reinikainen T, Ruohonen L, Pettersson G, Knowles JKC, Teeri TT, Jones TA (1994) The 3dimensional crystal-structure of the catalytic core of cellobiohydrolase-I from Trichoderma reesei. Science 265:524–528PubMedGoogle Scholar
  52. 52.
    Divne C, Ståhlberg J, Teeri TT, Jones TA (1998) High resolution crystal structures reveal how a cellulose chain is bound in the 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei. J Mol Biol 275:309–325PubMedGoogle Scholar
  53. 53.
    Kleywegt GJ, Zou JY, Divne C, Davies GJ, Sinning I, Ståhlberg J, Reinikainen T, Srisodsuk M, Teeri TT, Jones TA (1997) The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 Å resolution, and a comparison with related enzymes. J Mol Biol 272:383–397PubMedGoogle Scholar
  54. 54.
    Mackenzie LF, Sulzenbacher G, Divne C, Jones TA, Woldike HF, Schulein M, Withers SG, Davies GJ (1998) Crystal structure of the family 7 dndoglucanase 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 335:409–416PubMedPubMedCentralGoogle Scholar
  55. 55.
    Ståhlberg J, Johansson G, Pettersson G, New A (1991) Model for enzymatic-hydrolysis of cellulose based on the 2-domain structure of cellobiohydrolase-I. Biotechnol Biofuels 9:286–290Google Scholar
  56. 56.
    Payne CM, Baban J, Horn SJ, Backe PH, Arvai AS, Dalhus B, Bjørås M, Eijsink VGH, Sørlie M, Beckham GT et al (2012) Hallmarks of processivity in glycoside hydrolases from crystallographic and computational studies of the Serratia marcescens Chitinases. J Biol Chem 287:36322–36330PubMedPubMedCentralGoogle Scholar
  57. 57.
    Taylor CB, Payne CM, Himmel ME, Crowley MF, McCabe C, Beckham GT (2013) Binding site dynamics and aromatic-carbohydrate interactions in processive and non-processive family 7 glycoside hydrolases. J Phys Chem B 117:4924–4933PubMedGoogle Scholar
  58. 58.
    Payne CM, Resch MG, Chen L, Crowley MF, Himmel ME, Taylor 2nd LE, Sandgren M, Ståhlberg J, Stals I, Tan Z, Beckham GT (2013) Glycosylated linkers in multimodular lignocellulose-degrading enzymes dynamically bind to cellulose. Proc Natl Acad Sci U S A 110:14646–14651PubMedPubMedCentralGoogle Scholar
  59. 59.
    Mandelman D, Belaich A, Belaich JP, Aghajari N, Driguez H, Haser R (2003) X-ray crystal structure of the multidomain endoglucanase Cel9G from Clostridium cellulolyticum complexed with natural and synthetic cello-oligosaccharides. J Bacteriol 185(14):4127–4135PubMedPubMedCentralGoogle Scholar
  60. 60.
    Sakon J, Irwin D, Wilson DB, Karplus PA (1997) Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat Struct Biol 4(10):810–818PubMedGoogle Scholar
  61. 61.
    Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858PubMedPubMedCentralGoogle Scholar
  62. 62.
    Case DA, Cerutti DS, Cheatham III TE, Darden TA, Duke RE, Giese TJ, Gohlke H, Goetz AW, Greene D, Homeyer N, Izadi S, Kovalenko A, Lee TS, LeGrand S, Li P, Lin C, Liu J, Luchko T, Luo R, Mermelstein D, Merz KM, Monard G, Nguyen H, Omelyan I, Onufriev A, Pan F, Qi R, Roe DR, Roitberg A, Sagui C, Simmerling CL, Botello-Smith WM, Swails J, Walker RC, Wang J, Wolf RM, Wu X, Xiao L, York DM, Kollman PA (2017) AMBER 2017. University of California, San FranciscoGoogle Scholar
  63. 63.
    Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16):1781–1802PubMedPubMedCentralGoogle Scholar
  64. 64.
    Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(1):33–38 27-8PubMedPubMedCentralGoogle Scholar
  65. 65.
    Edgar RC (2004a) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113PubMedPubMedCentralGoogle Scholar
  66. 66.
    Edgar RC (2004b) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralGoogle Scholar
  67. 67.
    Grant BJ, Rodrigues AP, ElSawy KM, McCammon JA, Caves LS (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22:2695–2696PubMedGoogle Scholar
  68. 68.
    Altman RB, Gerstein M (1994) Finding an average core structure: application to the globins. Proc Int Conf Intell Syst Mol Biol 2:19–27PubMedGoogle Scholar
  69. 69.
    Gerstein M, Altman RB (1995) Average core structures and variability measures for protein families: application to the immunoglobulins. J Mol Biol 251(1):161–175PubMedGoogle Scholar
  70. 70.
    Gerstein M, Chothia C (1991) Analysis of protein loop closure. Two types of hinges produce one motion in lactate dehydrogenase. J Mol Biol 220(1):133–149PubMedGoogle Scholar
  71. 71.
    Durand P, Trinquier G, Sanejouand Y-H (1994) A new approach for determining low-frequency normal modes in macromolecules. Biopolymers 34(6):759–771Google Scholar
  72. 72.
    Hinsen K, Petrescu A-J, Dellerue S, Bellissent-Funel M-C, Kneller GR (2000) Harmonicity in slow protein dynamics. Chem Phys 261(1–2):25–37Google Scholar
  73. 73.
    Kaplan W, Littlejohn TG (2001) Swiss-PDB viewer (deep view). Brief Bioinform 2:195–197PubMedGoogle Scholar
  74. 74.
    Irwin JJ, Shoichet BK (2005) ZINC–a free database of commercially available compounds for virtual screening. J Chem Inf Model 45:177–182PubMedPubMedCentralGoogle Scholar
  75. 75.
    Irwin JJ, Sterling T, Mysinger MM, Bolstad ES, Coleman RG (2012) ZINC: a free tool to discover chemistry for biology. J Chem Inf Model:52, 1757–1768PubMedPubMedCentralGoogle Scholar
  76. 76.
    Das B, Meirovitch H, Navon IM (2003) Performance of hybrid methods for large-scale unconstrained optimization as applied to models of proteins. J Comput Chem 24(10):1222–1231PubMedGoogle Scholar
  77. 77.
    Rappe AK, Casewit CJ, Colwell KS, Goddard WA, Skiff WM (1992) UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations. J Am Chem Soc 114(25):10024–10035Google Scholar
  78. 78.
    Bikadi Z, Hazai E (2009) Application of the PM6 semi-empirical method to modeling proteins enhances docking accuracy of AutoDock. Aust J Chem 1:15Google Scholar
  79. 79.
    Stewart JJ (2009) Application of the PM6 method to modeling proteins. J Mol Model 15:765–805PubMedGoogle Scholar
  80. 80.
    Halgren TA (1996) Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J Comput Chem 17:490–519Google Scholar
  81. 81.
    Morris GM, Goodsell DS (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19(14):1639–1662Google Scholar
  82. 82.
    Solis FJ, Wets RJB (1981) Minimization by random search techniques. Math Oper Res 6(1):19–30Google Scholar
  83. 83.
    Urbanowicz BR, Catala C, Irwin D, Wilson DB, Ripoll DR, Rose JK (2007) A tomato endo-beta-1,4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules (CBM49). J Biol Chem 282(16):12066–12074PubMedGoogle Scholar
  84. 84.
    Buchanan M, Burton RA, Dhugga KS, Rafalski AJ, Tingey SV, Shirley NJ, Fincher GB (2012) Endo-(1,4)-beta-glucanase gene families in the grasses: temporal and spatial co-transcription of orthologous genes. BMC Plant Biol 12:235PubMedPubMedCentralGoogle Scholar
  85. 85.
    Xie G, Yang B, Xu Z, Li F, Guo K, Zhang M, Wang L, Zou W, Wang Y, Peng L (2013) Global identification of multiple OsGH9 family members and their involvement in cellulose crystallinity modification in rice. PLoS One 8:e50171PubMedPubMedCentralGoogle Scholar
  86. 86.
    van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW, Dunker AK, Fuxreiter M, Gough J, Gsponer J, Jones DT et al (2014) Classification of intrinsically disordered regions and proteins. Chem Rev 114(13):6589–6631PubMedPubMedCentralGoogle Scholar
  87. 87.
    van der Lee R, Lang B, Kruse K, Gsponer J, Sanchez de Groot N, Huynen MA, Matouschek A, Fuxreiter M, Babu MM (2014) Intrinsically disordered segments affect protein half-life in the cell and during evolution. Cell Rep 8(6):1832–1844PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiochemistryArmy College of Medical SciencesNew DelhiIndia

Personalised recommendations