Engineering the acceptor substrate specificity in the xyloglucan endotransglycosylase TmXET6.3 from nasturtium seeds (Tropaeolum majus L.)

  • Barbora Stratilová
  • Zuzana Firáková
  • Jaroslav Klaudiny
  • Sergej Šesták
  • Stanislav Kozmon
  • Dana Strouhalová
  • Soňa Garajová
  • Fairouz Ait-Mohand
  • Ágnes Horváthová
  • Vladimír Farkaš
  • Eva Stratilová
  • Maria HrmovaEmail author


Key message

The knowledge of substrate specificity of XET enzymes is important for the general understanding of metabolic pathways to challenge the established notion that these enzymes operate uniquely on cellulose-xyloglucan networks.


Xyloglucan xyloglucosyl transferases (XETs) (EC play a central role in loosening and re-arranging the cellulose-xyloglucan network, which is assumed to be the primary load-bearing structural component of plant cell walls. The sequence of mature TmXET6.3 from Tropaeolum majus (280 residues) was deduced by the nucleotide sequence analysis of complete cDNA by Rapid Amplification of cDNA Ends, based on tryptic and chymotryptic peptide sequences. Partly purified TmXET6.3, expressed in Pichia occurred in N-glycosylated and unglycosylated forms. The quantification of hetero-transglycosylation activities of TmXET6.3 revealed that (1,3;1,4)-, (1,6)- and (1,4)-β-d-glucooligosaccharides were the preferred acceptor substrates, while (1,4)-β-d-xylooligosaccharides, and arabinoxylo- and glucomanno-oligosaccharides were less preferred. The 3D model of TmXET6.3, and bioinformatics analyses of identified and putative plant xyloglucan endotransglycosylases (XETs)/hydrolases (XEHs) of the GH16 family revealed that H94, A104, Q108, K234 and K237 were the key residues that underpinned the acceptor substrate specificity of TmXET6.3. Compared to the wild-type enzyme, the single Q108R and K237T, and double-K234T/K237T and triple-H94Q/A104D/Q108R variants exhibited enhanced hetero-transglycosylation activities with xyloglucan and (1,4)-β-d-glucooligosaccharides, while those with (1,3;1,4)- and (1,6)-β-d-glucooligosaccharides were suppressed; the incorporation of xyloglucan to (1,4)-β-d-glucooligosaccharides by the H94Q variant was influenced most extensively. Structural and biochemical data of non-specific TmXET6.3 presented here extend the classic XET reaction mechanism by which these enzymes operate in plant cell walls. The evaluations of TmXET6.3 transglycosylation activities and the incidence of investigated residues in other members of the GH16 family suggest that a broad acceptor substrate specificity in plant XET enzymes could be more widespread than previously anticipated.


Bioinformatics GH16 family Homo- and hetero-transglycosylation Protein molecular modelling Site-directed mutagenesis 





















Carboxymethyl cellulose


Atomic colour scheme


TmXET6.3 without putative signal peptide


Penta-galacturonic acid oligosaccharide






Family 16 glycoside hydrolase


Hydroxyethyl cellulose


High performance liquid chromatography










Mixed-linkage (1,3;1,4)-β-d-gluco-saccharides


(1,3;1,4)-β-d-tetra-glucosaccharides A, B, C


Matrix-assisted laser desorption/ionisation


Mass spectrometry








Tropaeolum majus XET6.3


Rapid Amplification of cDNA Ends


Root-mean square deviation


Sodium dodecyl sulfate–polyacrylamide gel electrophoresis






Xyloglucan endo-(1,4)-β-d-glucanase


Xyloglucan endotransglycosylase/hydrolase




Xyloglucan heptasaccharide


Xyloglucan octasaccharide


Xyloglucan nonasaccharide


Xyloglucan oligosaccharides









This work was supported by the grant No. 2/0058/16 from VEGA, Slovakia to ES, and by the funding from Huaiyin Normal University and the Australian Research Council Linkage Project (DP120100900) to MH. We thank IBH Wilson from the Universität für Bodenkultur, Vienna, Austria, for providing the pPICZα-His/FLAG plasmid, to I Zelko and R Vadkertiova (Institute of Chemistry) for the assistance with fluorescent microscopy, and H Čigašová (Institute of Chemistry) for technical assistance.

Authors contributions

Conceived, designed experiments and analysed data: B.S., Z.F., J.K., S.Š., E.S. and M.H. Z.F. and J.K. determined the primary structure of TmXET6.3, B.S. and E.S. quantified enzyme activities of wild-type and variants, Á.H., B.S. and F.A-M. run electrophoretic analyses, E.S. conducted microscopy analyses, S.Š. constructed variant plasmids and selected hyper-producing clones, D.S. and S.G. worked out activity assays, S.K. built the 3D homology model, BS conducted large-scale bioinformatics analyses and suggested variant sites, V.F. prepared fluorescent oligosaccharides, M.H. conducted phylogeny reconstruction analyses and generated structural graphics. Discussed the data and contributed to writing: B.S., J.K., S.Š., S.K., V.F., E.S. and M.H. E.S. and M.H. designed research and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflict of interest.

Supplementary material

11103_2019_852_MOESM1_ESM.pdf (1.3 mb)
Supplementary material 1 (PDF 1370 KB)


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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Centre for Glycomics, Institute of ChemistrySlovak Academy of SciencesBratislavaSlovakia
  2. 2.Department of Physical and Theoretical Chemistry, Faculty of Natural SciencesComenius UniversityBratislavaSlovakia
  3. 3.Institute of Analytical ChemistryCzech Academy of SciencesBrnoCzech Republic
  4. 4.School of Life SciencesHuaiyin Normal UniversityHuai’anChina
  5. 5.School of Agriculture, Food and Wine, and Waite Research Institute, Waite Research PrecinctUniversity of AdelaideGlen OsmondAustralia

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