Abstract
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.
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Anders N et al (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci USA 109:989–993
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 764:156–166
Beaucage G (1995) Approximations leading to a unified exponential/power-law approach to small-angle scattering. J Appl Crystallogr 28:717–728
Beglov D, Roux B (1994) Finite representation of an infinite bulk system: solvent boundary potential for computer simulations. J Chem Phys 100:9050–9063
Berendsen HJC, van der Spoel D, van Drunen R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun 91:43–56
Bonomi M et al (2009) PLUMED: a portable plugin for free-energy calculations with molecular dynamics. Comput Phys Commun 180:1961–1972
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 15:924–930
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 79:492–506
Busse-Wicher M et al (2016) Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose. Plant Physiol 171:2418–2431
Bussi G (2013) Hamiltonian replica exchange in GROMACS: a flexible implementation. Mol Phys 112:379–384
Carpita NC (1983) Hemicellulosic polymers of cell walls of zea coleoptiles. Plant Physiol 72:515
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 57:2401–2406
Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092
Darvill JE, McNeil M, Darvill AG, Albersheim P (1980) Structure of plant cell walls. Plant Physiol 66:1135
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 54:724–728
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 26:108–114
Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593
Feller SE, Zhang Y, Pastor RW, Brooks BR (1995) Constant pressure molecular dynamics simulation: the Langevin piston method. J Chem Phys 103:4613–4621
Grantham NJ et al (2017) An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls. Nat Plants 3:859–865
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 29:2543–2564
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 5:2353–2370
Heller WT et al (2014) The Bio-SANS instrument at the high flux isotope reactor of Oak Ridge National Laboratory. J Appl Crystallogr 47:1238–1246
Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472
Ilavsky J, Jemian PR (2009) Irena: tool suite for modeling and analysis of small-angle scattering. J Appl Crystallogr 42:347–353
Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100:11783–11788
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926–935
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 69:94–105
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 12:2633–2641
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 72:650–654
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 385–386:880–882
Martinez-Abad A et al (2017) Regular motifs in xylan modulate molecular flexibility and interactions with cellulose surfaces. Plant Physiol 175:1579–1592
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 124:1–11
Martyna GJ, Tobias DJ, Klein ML (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101:4177–4189
McLean AD, Chandler GS (1980) Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z = 11–18. J Chem Phys 72:5639–5648
Mota FL, Queimada AJ, Pinho SP, Macedo EA (2008) Aqueous solubility of some natural phenolic compounds. Ind Eng Chem Res 47:5182–5189
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 124:9074–9082
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, Rijeka
Parrinello M, Rahman A (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52:7182–7190
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 18:1311–1321
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 89:2193–2218
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 94:6091–6101
Petridis L, Smith JC (2009) A molecular mechanics force field for lignin. J Comput Chem 30:457–467
Phillips JC et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802
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 10:1962–1969
Pronk S et al (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845–854
Roothaan CCJ (1951) New developments in molecular orbital theory. Rev Mod Phys 23:69–89
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 23:327–341
Selig MJ, Thygesen LG, Felby C, Master ER (2015) Debranching of soluble wheat arabinoxylan dramatically enhances recalcitrant binding to cellulose. Biotechnol Lett 37:633–641
Simmons TJ et al (2016) Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat Commun 7:13902
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 68:546–559
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 67:503–514
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 115:9431–9438
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 53:2840–2854
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 172:2107–2119
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 17:2210–2222
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 136:10399–10409
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 2:364–382
Acknowledgments
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.
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Shrestha, U.R., Smith, S., Pingali, S.V. et al. Arabinose substitution effect on xylan rigidity and self-aggregation. Cellulose 26, 2267–2278 (2019). https://doi.org/10.1007/s10570-018-2202-8
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DOI: https://doi.org/10.1007/s10570-018-2202-8