Arabinose substitution effect on xylan rigidity and self-aggregation

Utsab R. Shrestha, Sydney Smith, Sai Venkatesh Pingali, Hui Yang, Mai Zahran, Lloyd Breunig, Liza Anne Wilson, Malgorzata Kowalik, James D. Kubicki, Daniel J. Cosgrove, Hugh M. O’Neill, Loukas Petridis

Research output: Contribution to journalArticle

Abstract

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. Graphical abstract: [Figure not available: see fulltext.].

Original languageEnglish (US)
Pages (from-to)2267-2278
Number of pages12
JournalCellulose
Volume26
Issue number4
DOIs
StatePublished - Mar 15 2019

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Xylans
Arabinose
Cellulose
Rigidity
ferulic acid
Substitution reactions
Agglomeration
Acids
Glucuronic Acid
Xylose
Neutron scattering
Molecular dynamics
Esters
Mechanics
Entropy
Solubility
Cells
glucuronoarabinoxylan
Water
Computer simulation

All Science Journal Classification (ASJC) codes

  • Polymers and Plastics

Cite this

Shrestha, U. R., Smith, S., Pingali, S. V., Yang, H., Zahran, M., Breunig, L., ... Petridis, L. (2019). Arabinose substitution effect on xylan rigidity and self-aggregation. Cellulose, 26(4), 2267-2278. https://doi.org/10.1007/s10570-018-2202-8
Shrestha, Utsab R. ; Smith, Sydney ; Pingali, Sai Venkatesh ; Yang, Hui ; Zahran, Mai ; Breunig, Lloyd ; Wilson, Liza Anne ; Kowalik, Malgorzata ; Kubicki, James D. ; Cosgrove, Daniel J. ; O’Neill, Hugh M. ; Petridis, Loukas. / Arabinose substitution effect on xylan rigidity and self-aggregation. In: Cellulose. 2019 ; Vol. 26, No. 4. pp. 2267-2278.
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Shrestha, UR, Smith, S, Pingali, SV, Yang, H, Zahran, M, Breunig, L, Wilson, LA, Kowalik, M, Kubicki, JD, Cosgrove, DJ, O’Neill, HM & Petridis, L 2019, 'Arabinose substitution effect on xylan rigidity and self-aggregation', Cellulose, vol. 26, no. 4, pp. 2267-2278. https://doi.org/10.1007/s10570-018-2202-8

Arabinose substitution effect on xylan rigidity and self-aggregation. / Shrestha, Utsab R.; Smith, Sydney; Pingali, Sai Venkatesh; Yang, Hui; Zahran, Mai; Breunig, Lloyd; Wilson, Liza Anne; Kowalik, Malgorzata; Kubicki, James D.; Cosgrove, Daniel J.; O’Neill, Hugh M.; Petridis, Loukas.

In: Cellulose, Vol. 26, No. 4, 15.03.2019, p. 2267-2278.

Research output: Contribution to journalArticle

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T1 - Arabinose substitution effect on xylan rigidity and self-aggregation

AU - Shrestha, Utsab R.

AU - Smith, Sydney

AU - Pingali, Sai Venkatesh

AU - Yang, Hui

AU - Zahran, Mai

AU - Breunig, Lloyd

AU - Wilson, Liza Anne

AU - Kowalik, Malgorzata

AU - Kubicki, James D.

AU - Cosgrove, Daniel J.

AU - O’Neill, Hugh M.

AU - Petridis, Loukas

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N2 - 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. Graphical abstract: [Figure not available: see fulltext.].

AB - 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. Graphical abstract: [Figure not available: see fulltext.].

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Shrestha UR, Smith S, Pingali SV, Yang H, Zahran M, Breunig L et al. Arabinose substitution effect on xylan rigidity and self-aggregation. Cellulose. 2019 Mar 15;26(4):2267-2278. https://doi.org/10.1007/s10570-018-2202-8