, Volume 26, Issue 4, pp 2267–2278 | Cite as

Arabinose substitution effect on xylan rigidity and self-aggregation

  • Utsab R. Shrestha
  • Sydney Smith
  • Sai Venkatesh Pingali
  • Hui Yang
  • Mai Zahran
  • Lloyd Breunig
  • Liza A. Wilson
  • Margaret Kowali
  • James D. Kubicki
  • Daniel J. Cosgrove
  • Hugh M. O’Neill
  • Loukas PetridisEmail author
Original Research


Substituted xylans play an important role in the structure and mechanics of the primary cell wall of plants. Arabinoxylans (AX) consist of a xylose backbone substituted with arabinose, while glucuronoarabinoxylans (GAX) also contain glucuronic acid substitutions and ferulic acid esters on some of the arabinoses. We provide a molecular-level description on the dependence of xylan conformational, self-aggregation properties and binding to cellulose on the degree of arabinose substitution. Molecular dynamics simulations reveal fully solubilized xylans with a low degree of arabinose substitution (lsAX) to be stiffer than their highly substituted (hsAX) counterparts. Small-angle neutron scattering experiments indicate that both wild-type hsAX and debranched lsAX form macromolecular networks that are penetrated by water. In those networks, lsAX are more folded and entangled than hsAX chains. Increased conformational entropy upon network formation for hsAX contributes to AX loss of solubility upon debranching. Furthermore, simulations show the intermolecular contacts to cellulose are not affected by arabinose substitution (within the margin of error). Ferulic acid is the GAX moiety found here to bind to cellulose most strongly, suggesting it may play an anchoring role to strengthen GAX-cellulose interactions. The above results suggest highly substituted GAX acts as a spacer, keeping cellulose microfibrils apart, whereas low substitution GAX is more localized in plant cell walls and promotes cellulose bundling.

Graphical abstract


Plant cell wall Xylan Molecular simulation Neutron scattering 



This research was supported by the Center for Lignocellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences under Award DE-SC0001090. This research used resources of two DOE Office of Science User Facilities: the National Energy Research Scientific Computing Center, a supported under Contract No. DE-AC02-05CH11231, and the High Flux Isotope Reactor at Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U. S. Department of Energy under Contract DE-AC05-00OR22725.

Compliance with ethical standards

Conflict of interest

There are no conflicts to declare.

Supplementary material

10570_2018_2202_MOESM1_ESM.pdf (757 kb)
Supplementary material 1 (PDF 757 kb)


  1. Anders N et al (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci USA 109:989–993CrossRefGoogle Scholar
  2. Arnold O et al (2014) Mantid—data analysis and visualization package for neutron scattering and μ SR experiments. Nucl Instr Meth Phys Res Sect A: Accel Spectrom Detect Assoc Equip 764:156–166CrossRefGoogle Scholar
  3. Beaucage G (1995) Approximations leading to a unified exponential/power-law approach to small-angle scattering. J Appl Crystallogr 28:717–728CrossRefGoogle Scholar
  4. Beglov D, Roux B (1994) Finite representation of an infinite bulk system: solvent boundary potential for computer simulations. J Chem Phys 100:9050–9063CrossRefGoogle Scholar
  5. Berendsen HJC, van der Spoel D, van Drunen R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun 91:43–56CrossRefGoogle Scholar
  6. Bonomi M et al (2009) PLUMED: a portable plugin for free-energy calculations with molecular dynamics. Comput Phys Commun 180:1961–1972CrossRefGoogle Scholar
  7. Bosmans TJ, Stepan AM, Toriz G, Renneckar S, Karabulut E, Wagberg L, Gatenholm P (2014) Assembly of debranched xylan from solution and on nanocellulosic surfaces. Biomacromolecules 15:924–930CrossRefGoogle Scholar
  8. Busse-Wicher M et al (2014) The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J 79:492–506CrossRefGoogle Scholar
  9. Busse-Wicher M et al (2016) Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose. Plant Physiol 171:2418–2431Google Scholar
  10. Bussi G (2013) Hamiltonian replica exchange in GROMACS: a flexible implementation. Mol Phys 112:379–384CrossRefGoogle Scholar
  11. Carpita NC (1983) Hemicellulosic polymers of cell walls of zea coleoptiles. Plant Physiol 72:515CrossRefGoogle Scholar
  12. Danne R, Poojari C, Martinez-Seara H, Rissanen S, Lolicato F, Rog T, Vattulainen I (2017) doGlycans-Tools for preparing carbohydrate structures for atomistic simulations of glycoproteins, glycolipids, and carbohydrate polymers for GROMACS. J Chem Inf Model 57:2401–2406CrossRefGoogle Scholar
  13. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092CrossRefGoogle Scholar
  14. Darvill JE, McNeil M, Darvill AG, Albersheim P (1980) Structure of plant cell walls. Plant Physiol 66:1135CrossRefGoogle Scholar
  15. Ditchfield R, Hehre WJ, Pople JA (1971) Self-consistent molecular-orbital methods. IX. An extended Gaussian-type basis for molecular-orbital studies of organic molecules. J Chem Phys 54:724–728CrossRefGoogle Scholar
  16. Doblin MS, Johnson KL, Humphries J, Newbigin EJ, Bacic A (2014) Are designer plant cell walls a realistic aspiration or will the plasticity of the plant’s metabolism win out? Curr Opin Biotechnol 26:108–114CrossRefGoogle Scholar
  17. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593CrossRefGoogle Scholar
  18. Feller SE, Zhang Y, Pastor RW, Brooks BR (1995) Constant pressure molecular dynamics simulation: the Langevin piston method. J Chem Phys 103:4613–4621CrossRefGoogle Scholar
  19. Grantham NJ et al (2017) An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls. Nat Plants 3:859–865CrossRefGoogle Scholar
  20. Guvench O, Greene SN, Kamath G, Brady JW, Venable RM, Pastor RW, Mackerell AD (2008) Additive empirical force field for hexopyranose monosaccharides. J Comput Chem 29:2543–2564CrossRefGoogle Scholar
  21. Guvench O, Hatcher E, Venable RM, Pastor RW, MacKerell AD (2009) CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses. J Chem Theory Comput 5:2353–2370CrossRefGoogle Scholar
  22. Heller WT et al (2014) The Bio-SANS instrument at the high flux isotope reactor of Oak Ridge National Laboratory. J Appl Crystallogr 47:1238–1246CrossRefGoogle Scholar
  23. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472CrossRefGoogle Scholar
  24. Ilavsky J, Jemian PR (2009) Irena: tool suite for modeling and analysis of small-angle scattering. J Appl Crystallogr 42:347–353CrossRefGoogle Scholar
  25. Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100:11783–11788CrossRefGoogle Scholar
  26. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926–935CrossRefGoogle Scholar
  27. Kabel MA, van den Borne H, Vincken J-P, Voragen AGJ, Schols HA (2007) Structural differences of xylans affect their interaction with cellulose. Carbohydr Polym 69:94–105CrossRefGoogle Scholar
  28. Köhnke T, Östlund Å, Brelid H (2011) Adsorption of arabinoxylan on cellulosic surfaces: influence of degree of substitution and substitution pattern on adsorption characteristics. Biomacromolecules 12:2633–2641CrossRefGoogle Scholar
  29. Krishnan R, Binkley JS, Seeger R, Pople JA (1980) Self-consistent molecular orbital methods. XX. A basis set for correlated wave functions. J Chem Phys 72:650–654CrossRefGoogle Scholar
  30. Lynn GW, Heller W, Urban V, Wignall GD, Weiss K, Myles DAA (2006) Bio-SANS—a dedicated facility for neutron structural biology at Oak Ridge National Laboratory. Physica B 385–386:880–882CrossRefGoogle Scholar
  31. Martinez-Abad A et al (2017) Regular motifs in xylan modulate molecular flexibility and interactions with cellulose surfaces. Plant Physiol 175:1579–1592CrossRefGoogle Scholar
  32. Martinez-Sanz M, Mikkelsen D, Flanagan BM, Gidley MJ, Gilbert EP (2017) Multi-scale characterisation of deuterated cellulose composite hydrogels reveals evidence for different interaction mechanisms with arabinoxylan, mixed-linkage glucan and xyloglucan. Polymer 124:1–11CrossRefGoogle Scholar
  33. Martyna GJ, Tobias DJ, Klein ML (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101:4177–4189CrossRefGoogle Scholar
  34. McLean AD, Chandler GS (1980) Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z = 11–18. J Chem Phys 72:5639–5648CrossRefGoogle Scholar
  35. Mota FL, Queimada AJ, Pinho SP, Macedo EA (2008) Aqueous solubility of some natural phenolic compounds. Ind Eng Chem Res 47:5182–5189CrossRefGoogle Scholar
  36. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron x-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082CrossRefGoogle Scholar
  37. Ochoa-Villarreal M, Aispuro-Hernández E, Vargas-Arispuro I, Martínez-Téllez MÁ (2012) Plant cell wall polymers: function, structure and biological activity of their derivatives. In: Gomes ADS (ed) Polymerization. InTech, RijekaGoogle Scholar
  38. Parrinello M, Rahman A (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52:7182–7190CrossRefGoogle Scholar
  39. Pereira CS, Silveira RL, Dupree P, Skaf MS (2017) Effects of xylan side-chain substitutions on xylan–cellulose interactions and implications for thermal pretreatment of cellulosic biomass. Biomacromolecules 18:1311–1321CrossRefGoogle Scholar
  40. Petersson GA, Bennett A, Tensfeldt TG, Al-Laham MA, Shirley WA, Mantzaris J (1988) A complete basis set model chemistry. I. The total energies of closed-shell atoms and hydrides of the first-row elements. J Chem Phys 89:2193–2218CrossRefGoogle Scholar
  41. Petersson GA, Tensfeldt TG, Montgomery JA (1991) A complete basis set model chemistry. III. The complete basis set-quadratic configuration interaction family of methods. J Chem Phys 94:6091–6101CrossRefGoogle Scholar
  42. Petridis L, Smith JC (2009) A molecular mechanics force field for lignin. J Comput Chem 30:457–467CrossRefGoogle Scholar
  43. Phillips JC et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802CrossRefGoogle Scholar
  44. Pitkanen L, Virkki L, Tenkanen M, Tuomainen P (2009) Comprehensive multidetector HPSEC study on solution properties of cereal arabinoxylans in aqueous and DMSO solutions. Biomacromolecules 10:1962–1969CrossRefGoogle Scholar
  45. Pronk S et al (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845–854CrossRefGoogle Scholar
  46. Roothaan CCJ (1951) New developments in molecular orbital theory. Rev Mod Phys 23:69–89CrossRefGoogle Scholar
  47. Ryckaert J-P, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23:327–341CrossRefGoogle Scholar
  48. Selig MJ, Thygesen LG, Felby C, Master ER (2015) Debranching of soluble wheat arabinoxylan dramatically enhances recalcitrant binding to cellulose. Biotechnol Lett 37:633–641CrossRefGoogle Scholar
  49. Simmons TJ et al (2016) Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat Commun 7:13902CrossRefGoogle Scholar
  50. Tabuchi A, Li L-C, Cosgrove DJ (2011) Matrix solubilization and cell wall weakening by β-expansin (group-1 allergen) from maize pollen. Plant J 68:546–559CrossRefGoogle Scholar
  51. Wang T, Hong M (2016) Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J Exp Bot 67:503–514CrossRefGoogle Scholar
  52. Wang L, Friesner RA, Berne BJ (2011) Replica exchange with solute scaling: a more efficient version of replica exchange with solute tempering (REST2). J Phys Chem B 115:9431–9438CrossRefGoogle Scholar
  53. Wang T, Salazar A, Zabotina OA, Hong M (2014) Structure and dynamics of brachypodium primary cell wall polysaccharides from two-dimensional 13C solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53:2840–2854CrossRefGoogle Scholar
  54. Wang T, Chen Y, Tabuchi A, Hong M, Cosgrove DJ (2016a) The target of β-expansin EXPB1 in maize cell walls from binding and solid-state NMR studies. Plant Physiol 172:2107–2119CrossRefGoogle Scholar
  55. Wang T, Yang H, Kubicki JD, Hong M (2016b) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17:2210–2222CrossRefGoogle Scholar
  56. White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water–polysaccharide interactions in the primary cell wall of arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136:10399–10409CrossRefGoogle Scholar
  57. Zhao Y, Schultz NE, Truhlar DG (2006) Design of density functionals by combining the method of constraint satisfaction with parametrization for thermochemistry, thermochemical kinetics, and noncovalent interactions. J Chem Theory Comput 2:364–382CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  • Utsab R. Shrestha
    • 1
  • Sydney Smith
    • 1
  • Sai Venkatesh Pingali
    • 2
  • Hui Yang
    • 3
  • Mai Zahran
    • 4
  • Lloyd Breunig
    • 3
  • Liza A. Wilson
    • 3
  • Margaret Kowali
    • 5
  • James D. Kubicki
    • 6
  • Daniel J. Cosgrove
    • 3
  • Hugh M. O’Neill
    • 2
  • Loukas Petridis
    • 1
    Email author
  1. 1.UT/ORNL Center for Molecular BiophysicsOak Ridge National LaboratoryOak RidgeUSA
  2. 2.Neutron Scattering DivisionOak Ridge National LaboratoryOak RidgeUSA
  3. 3.Department of BiologyPennsylvania State UniversityUniversity ParkUSA
  4. 4.Department of BiologyNew York City College of TechnologyNew YorkUSA
  5. 5.Department of Chemical EngineeringPennsylvania State UniversityUniversity ParkUSA
  6. 6.Department of Geological SciencesUniversity of Texas at El PasoEl PasoUSA

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