Hetero-trans-β-glucanase, an enzyme unique to Equisetum plants, functionalises cellulose

Thomas J. Simmons, Kyle E. Mohler, Claire Holland, Florence Goubet, Lenka Franková, Douglas R. Houston, Andrew D. Hudson, Frank Meulewaeter, Stephen C. Fry*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Cell walls are metabolically active components of plant cells. They contain diverse enzymes, including transglycanases (endotransglycosylases) - enzymes that 'cut and paste' certain structural polysaccharide molecules and thus potentially remodel the wall during growth and development. Known transglycanase activities can modify several cell-wall polysaccharides [xyloglucan, mannans, mixed-linkage β-glucan (MLG) and xylans]; however, no transglycanases were known to act on cellulose, the principal polysaccharide of biomass. We now report the discovery in horsetails (Equisetum spp., an early-diverging genus of monilophytes), and characterisation, of hetero-trans-β-glucanase (HTG), a transglycanase that targets cellulose. HTG is also remarkable in predominantly catalysing hetero-transglycosylation: its preferred donor-substrates (cellulose or MLG) differ qualitatively from its acceptor-substrate (xyloglucan). HTG thus generates stable cellulose-xyloglucan and MLG-xyloglucan covalent bonds, and may thereby strengthen ageing Equisetum tissues by inter-linking different structural polysaccharides of the cell wall. 3D-modelling suggests that only three key amino acid substitutions (Trp → Pro, Gly → Ser, and Arg → Leu) were responsible for the evolution of HTG's unique specificity from the better-known xyloglucan-acting homo-transglycanases [xyloglucan endotransglucosylase/hydrolases (XTHs)]. Among land-plants, HTG appears to be confined to Equisetum, but its target polysaccharides are widespread, potentially offering opportunities for enhancing crop mechanical properties such as wind resistance. In addition, by linking cellulose to xyloglucan fragments previously tagged with compounds such as dyes or indicators, HTG may be useful biotechnologically for manufacturing stably functionalised celluloses, thereby potentially offering a commercially valuable 'green' technology for industrially manipulating biomass.

Original languageEnglish
Pages (from-to)753-769
Number of pages17
JournalThe Plant Journal
Volume83
Issue number5
Early online date17 Jul 2015
DOIs
Publication statusPublished - 1 Sep 2015

Keywords

  • cellulose
  • enzyme evolution
  • Equisetum
  • hemicelluloses
  • hetero-transglycanase
  • plant cell wall
  • transglycosylation

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