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Title: Analyzing Xyloglucan Endotransglycosylases by Incorporating Synthetic Oligosaccharides into Plant Cell Walls

Abstract

Abstract The plant cell wall is a cellular exoskeleton consisting predominantly of a complex polysaccharide network that defines the shape of cells. During growth, this network can be loosened through the action of xyloglucan endotransglycosylases (XETs), glycoside hydrolases that “cut and paste” xyloglucan polysaccharides through a transglycosylation process. We have analyzed cohorts of XETs in different plant species to evaluate the substrate specificities of xyloglucan acceptors by using a set of synthetic oligosaccharides obtained by automated glycan assembly. The ability of XETs to incorporate the oligosaccharides into polysaccharides printed as microarrays and into stem sections of Arabidopsis thaliana , beans, and peas was assessed. We found that single xylose substitutions are sufficient for transfer, and xylosylation of the terminal glucose residue is not required by XETs, independent of plant species. To obtain information on the potential xylosylation pattern of the natural acceptor of XETs, that is, the nonreducing end of xyloglucan, we further tested the activity of xyloglucan xylosyl transferase (XXT) 2 on the synthetic xyloglucan oligosaccharides. These data shed light on inconsistencies between previous studies towards determining the acceptor substrate specificities of XETs and have important implications for further understanding plant cell wall polysaccharide synthesis and remodeling.

Authors:
 [1];  [1];  [2];  [2]; ORCiD logo [1]
  1. Department of Biomolecular Systems Max Planck Institute of Colloids and Interfaces Am Mühlenberg 1 14476 Potsdam Germany, Freie Universität Berlin Institute of Chemistry and Biochemistry Arnimallee 22 14195 Berlin Germany
  2. Complex Carbohydrate Research Center University of Georgia 315 Riverbend Road Athens GA 30602 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1422455
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
ChemBioChem: a European journal of chemical biology
Additional Journal Information:
Journal Name: ChemBioChem: a European journal of chemical biology Journal Volume: 19 Journal Issue: 8; Journal ID: ISSN 1439-4227
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
France
Language:
English

Citation Formats

Ruprecht, Colin, Dallabernardina, Pietro, Smith, Peter J., Urbanowicz, Breeanna R., and Pfrengle, Fabian. Analyzing Xyloglucan Endotransglycosylases by Incorporating Synthetic Oligosaccharides into Plant Cell Walls. France: N. p., 2018. Web. doi:10.1002/cbic.201700638.
Ruprecht, Colin, Dallabernardina, Pietro, Smith, Peter J., Urbanowicz, Breeanna R., & Pfrengle, Fabian. Analyzing Xyloglucan Endotransglycosylases by Incorporating Synthetic Oligosaccharides into Plant Cell Walls. France. https://doi.org/10.1002/cbic.201700638
Ruprecht, Colin, Dallabernardina, Pietro, Smith, Peter J., Urbanowicz, Breeanna R., and Pfrengle, Fabian. Fri . "Analyzing Xyloglucan Endotransglycosylases by Incorporating Synthetic Oligosaccharides into Plant Cell Walls". France. https://doi.org/10.1002/cbic.201700638.
@article{osti_1422455,
title = {Analyzing Xyloglucan Endotransglycosylases by Incorporating Synthetic Oligosaccharides into Plant Cell Walls},
author = {Ruprecht, Colin and Dallabernardina, Pietro and Smith, Peter J. and Urbanowicz, Breeanna R. and Pfrengle, Fabian},
abstractNote = {Abstract The plant cell wall is a cellular exoskeleton consisting predominantly of a complex polysaccharide network that defines the shape of cells. During growth, this network can be loosened through the action of xyloglucan endotransglycosylases (XETs), glycoside hydrolases that “cut and paste” xyloglucan polysaccharides through a transglycosylation process. We have analyzed cohorts of XETs in different plant species to evaluate the substrate specificities of xyloglucan acceptors by using a set of synthetic oligosaccharides obtained by automated glycan assembly. The ability of XETs to incorporate the oligosaccharides into polysaccharides printed as microarrays and into stem sections of Arabidopsis thaliana , beans, and peas was assessed. We found that single xylose substitutions are sufficient for transfer, and xylosylation of the terminal glucose residue is not required by XETs, independent of plant species. To obtain information on the potential xylosylation pattern of the natural acceptor of XETs, that is, the nonreducing end of xyloglucan, we further tested the activity of xyloglucan xylosyl transferase (XXT) 2 on the synthetic xyloglucan oligosaccharides. These data shed light on inconsistencies between previous studies towards determining the acceptor substrate specificities of XETs and have important implications for further understanding plant cell wall polysaccharide synthesis and remodeling.},
doi = {10.1002/cbic.201700638},
journal = {ChemBioChem: a European journal of chemical biology},
number = 8,
volume = 19,
place = {France},
year = {Fri Feb 23 00:00:00 EST 2018},
month = {Fri Feb 23 00:00:00 EST 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1002/cbic.201700638

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Cited by: 11 works
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Works referenced in this record:

Mannan transglycosylase: a novel enzyme activity in cell walls of higher plants
journal, April 2004


Soluble and Membrane-Bound β-Glucosidases Are Involved in Trimming the Xyloglucan Backbone
journal, December 2016

  • Sampedro, Javier; Valdivia, Elene R.; Fraga, Patricia
  • Plant Physiology, Vol. 173, Issue 2
  • DOI: 10.1104/pp.16.01713

A Synthetic Glycan Microarray Enables Epitope Mapping of Plant Cell Wall Glycan-Directed Antibodies
journal, September 2017

  • Ruprecht, Colin; Bartetzko, Max P.; Senf, Deborah
  • Plant Physiology, Vol. 175, Issue 3
  • DOI: 10.1104/pp.17.00737

Biosynthesis of the Plant Cell Wall Matrix Polysaccharide Xyloglucan
journal, April 2016


Polysaccharide microarrays for high-throughput screening of transglycosylase activities in plant extracts
journal, December 2009

  • Kosík, Ondřej; Auburn, Richard P.; Russell, Steven
  • Glycoconjugate Journal, Vol. 27, Issue 1
  • DOI: 10.1007/s10719-009-9271-8

An unambiguous nomenclature for xyloglucan-derived oligosaccharides
journal, September 1993


Automated glycan assembly of xyloglucan oligosaccharides
journal, January 2016

  • Dallabernardina, Pietro; Schuhmacher, Frank; Seeberger, Peter H.
  • Organic & Biomolecular Chemistry, Vol. 14, Issue 1
  • DOI: 10.1039/C5OB02226F

XTH acts at the microfibril-matrix interface during cell elongation
journal, January 2005

  • Vissenberg, K.
  • Journal of Experimental Botany, Vol. 56, Issue 412
  • DOI: 10.1093/jxb/eri048

Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature
journal, January 2015


Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants
journal, March 1992

  • Fry, S. C.; Smith, R. C.; Renwick, K. F.
  • Biochemical Journal, Vol. 282, Issue 3
  • DOI: 10.1042/bj2820821

In Vivo Colocalization of Xyloglucan Endotransglycosylase Activity and Its Donor Substrate in the Elongation Zone of Arabidopsis Roots
journal, July 2000

  • Vissenberg, Kris; Martinez-Vilchez, Immaculada M.; Verbelen, Jean-Pierre
  • The Plant Cell, Vol. 12, Issue 7
  • DOI: 10.1105/tpc.12.7.1229

Xyloglucan Endotransglucosylase Activity Loosens a Plant Cell Wall
journal, October 2007

  • Van Sandt, Vicky S. T.; Suslov, Dmitry; Verbelen, Jean-Pierre
  • Annals of Botany, Vol. 100, Issue 7
  • DOI: 10.1093/aob/mcm248

Oligosaccharides as Signals and Substrates in the Plant Cell Wall
journal, September 1993

  • Fry, S. C.; Aldington, S.; Hetherington, P. R.
  • Plant Physiology, Vol. 103, Issue 1
  • DOI: 10.1104/pp.103.1.1

Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments
journal, June 2002

  • Takeda, T.; Furuta, Y.; Awano, T.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 13
  • DOI: 10.1073/pnas.132080299

Active-site Mapping of a Populus Xyloglucan endo -Transglycosylase with a Library of Xylogluco-oligosaccharides
journal, May 2008

  • Saura-Valls, Marc; Fauré, Régis; Brumer, Harry
  • Journal of Biological Chemistry, Vol. 283, Issue 32
  • DOI: 10.1074/jbc.M803058200

An Arabidopsis gene encoding an  -xylosyltransferase involved in xyloglucan biosynthesis
journal, May 2002

  • Faik, A.; Price, N. J.; Raikhel, N. V.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 11
  • DOI: 10.1073/pnas.102644799

Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746

Hetero-trans-β-glucanase, an enzyme unique to Equisetum plants, functionalizes cellulose
journal, August 2015

  • Simmons, Thomas J.; Mohler, Kyle E.; Holland, Claire
  • The Plant Journal, Vol. 83, Issue 5
  • DOI: 10.1111/tpj.12935

Synthesis of a Library of Xylogluco-Oligosaccharides for Active-Site Mapping of Xyloglucan endo -Transglycosylase
journal, July 2006

  • Fauré, Régis; Saura-Valls, Marc; Brumer, Harry
  • The Journal of Organic Chemistry, Vol. 71, Issue 14
  • DOI: 10.1021/jo0525682

Crystal Structures of a Poplar Xyloglucan Endotransglycosylase Reveal Details of Transglycosylation Acceptor Binding
journal, March 2004

  • Johansson, Patrik; Brumer, Harry; Baumann, Martin J.
  • The Plant Cell, Vol. 16, Issue 4
  • DOI: 10.1105/tpc.020065

Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism
journal, August 2017

  • Urbanowicz, Breeanna R.; Bharadwaj, Vivek S.; Alahuhta, Markus
  • The Plant Journal, Vol. 91, Issue 6
  • DOI: 10.1111/tpj.13628

Poplar Carbohydrate-Active Enzymes. Gene Identification and Expression Analyses
journal, January 2006

  • Geisler-Lee, Jane; Geisler, Matt; Coutinho, Pedro M.
  • Plant Physiology, Vol. 140, Issue 3
  • DOI: 10.1104/pp.105.072652

A Barley Xyloglucan Xyloglucosyl Transferase Covalently Links Xyloglucan, Cellulosic Substrates, and (1,3;1,4)-β-D-Glucans
journal, February 2007

  • Hrmova, Maria; Farkas, Vladimir; Lahnstein, Jelle
  • Journal of Biological Chemistry, Vol. 282, Issue 17
  • DOI: 10.1074/jbc.M611487200

Enzymatic Activity of Xyloglucan Xylosyltransferase 5
journal, May 2016

  • Culbertson, Alan T.; Chou, Yi-Hsiang; Smith, Adrienne L.
  • Plant Physiology, Vol. 171, Issue 3
  • DOI: 10.1104/pp.16.00361

Xyloglucan Endotransglycosylases Have a Function during the Formation of Secondary Cell Walls of Vascular Tissues
journal, November 2002

  • Bourquin, Veronica; Nishikubo, Nobuyuki; Abe, Hisashi
  • The Plant Cell, Vol. 14, Issue 12
  • DOI: 10.1105/tpc.007773

Active Site Mapping of Xylan-Deconstructing Enzymes with Arabinoxylan Oligosaccharides Produced by Automated Glycan Assembly
journal, February 2017

  • Senf, Deborah; Ruprecht, Colin; de Kruijff, Goswinus H. M.
  • Chemistry - A European Journal, Vol. 23, Issue 13
  • DOI: 10.1002/chem.201605902

Biochemistry and physiological roles of enzymes that ‘cut and paste’ plant cell-wall polysaccharides
journal, August 2013

  • Franková, Lenka; Fry, Stephen C.
  • Journal of Experimental Botany, Vol. 64, Issue 12
  • DOI: 10.1093/jxb/ert201

Microbial glycan microarrays define key features of host-microbial interactions
journal, May 2014

  • Stowell, Sean R.; Arthur, Connie M.; McBride, Ryan
  • Nature Chemical Biology, Vol. 10, Issue 6
  • DOI: 10.1038/nchembio.1525

Cleavage of xyloglucan by nasturtium seed xyloglucanase and transglycosylation to xyloglucan subunit oligosaccharides
journal, November 1992

  • Farkas, Vladimir; Sulova, Zdena; Stratilova, Eva
  • Archives of Biochemistry and Biophysics, Vol. 298, Issue 2
  • DOI: 10.1016/0003-9861(92)90423-T

Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood
journal, October 2014

  • Derba-Maceluch, Marta; Awano, Tatsuya; Takahashi, Junko
  • New Phytologist, Vol. 205, Issue 2
  • DOI: 10.1111/nph.13099

The XTH Gene Family: An Update on Enzyme Structure, Function, and Phylogeny in Xyloglucan Remodeling
journal, April 2010


Incorporation of β-(1,6)-linked glucooligosaccharides (pustulooligosaccharides) into plant cell wall structures
journal, January 2012


Automated glycan assembly of galactosylated xyloglucan oligosaccharides and their recognition by plant cell wall glycan-directed antibodies
journal, January 2017

  • Dallabernardina, Pietro; Ruprecht, Colin; Smith, Peter J.
  • Organic & Biomolecular Chemistry, Vol. 15, Issue 47
  • DOI: 10.1039/C7OB02605F

The XTH Family of Enzymes Involved in Xyloglucan Endotransglucosylation and Endohydrolysis: Current Perspectives and a New Unifying Nomenclature
journal, December 2002

  • Rose, Jocelyn K. C.; Braam, Janet; Fry, Stephen C.
  • Plant and Cell Physiology, Vol. 43, Issue 12
  • DOI: 10.1093/pcp/pcf171

Re-constructing our models of cellulose and primary cell wall assembly
journal, December 2014


An enzyme activity capable of endotransglycosylation of heteroxylan polysaccharides is present in plant primary cell walls
journal, September 2012


Two Xyloglucan Xylosyltransferases Catalyze the Addition of Multiple Xylosyl Residues to Cellohexaose
journal, September 2006

  • Cavalier, David M.; Keegstra, Kenneth
  • Journal of Biological Chemistry, Vol. 281, Issue 45
  • DOI: 10.1074/jbc.M606379200