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Title: Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism

Abstract

Summary The mechanistic underpinnings of the complex process of plant polysaccharide biosynthesis are poorly understood, largely because of the resistance of glycosyltransferase (GT) enzymes to structural characterization. In Arabidopsis thaliana, a glycosyl transferase family 37 (GT37) fucosyltransferase 1 ( At FUT1) catalyzes the regiospecific transfer of terminal 1,2‐fucosyl residues to xyloglucan side chains – a key step in the biosynthesis of fucosylated sidechains of galactoxyloglucan. We unravel the mechanistic basis for fucosylation by At FUT1 with a multipronged approach involving protein expression, X‐ray crystallography, mutagenesis experiments and molecular simulations. Mammalian cell culture expressions enable the sufficient production of the enzyme for X‐ray crystallography, which reveals the structural architecture of At FUT1 in complex with bound donor and acceptor substrate analogs. The lack of an appropriately positioned active site residue as a catalytic base leads us to propose an atypical water‐mediated fucosylation mechanism facilitated by an H‐bonded network, which is corroborated by mutagenesis experiments as well as detailed atomistic simulations.

Authors:
 [1]; ORCiD logo [2];  [2];  [1];  [2];  [2];  [1];  [1];  [3];  [2];  [1];  [1];  [2]
  1. Univ. of Georgia, Athens, GA (United States)
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  3. Univ. of Georgia, Athens, GA (United States); Univ. of California San Francisco, San Francisco, CA (United States)
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1389734
Alternate Identifier(s):
OSTI ID: 1377643
Report Number(s):
NREL/JA-2700-67766
Journal ID: ISSN 0960-7412
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 91; Journal Issue: 6; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; Arabidopsis thaliana; fucosylation; hemicellulose synthesis; fucosyltransferase; reaction mechanism

Citation Formats

Urbanowicz, Breeanna R., Bharadwaj, Vivek S., Alahuhta, Markus, Pena, Maria J., Lunin, Vladimir V., Bomble, Yannick J., Wang, Shuo, Yang, Jeong -Yeh, Tuomivaara, Sami T., Himmel, Michael E., Moremen, Kelley W., York, William S., and Crowley, Michael F. Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism. United States: N. p., 2017. Web. doi:10.1111/tpj.13628.
Urbanowicz, Breeanna R., Bharadwaj, Vivek S., Alahuhta, Markus, Pena, Maria J., Lunin, Vladimir V., Bomble, Yannick J., Wang, Shuo, Yang, Jeong -Yeh, Tuomivaara, Sami T., Himmel, Michael E., Moremen, Kelley W., York, William S., & Crowley, Michael F. Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism. United States. https://doi.org/10.1111/tpj.13628
Urbanowicz, Breeanna R., Bharadwaj, Vivek S., Alahuhta, Markus, Pena, Maria J., Lunin, Vladimir V., Bomble, Yannick J., Wang, Shuo, Yang, Jeong -Yeh, Tuomivaara, Sami T., Himmel, Michael E., Moremen, Kelley W., York, William S., and Crowley, Michael F. Mon . "Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism". United States. https://doi.org/10.1111/tpj.13628. https://www.osti.gov/servlets/purl/1389734.
@article{osti_1389734,
title = {Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism},
author = {Urbanowicz, Breeanna R. and Bharadwaj, Vivek S. and Alahuhta, Markus and Pena, Maria J. and Lunin, Vladimir V. and Bomble, Yannick J. and Wang, Shuo and Yang, Jeong -Yeh and Tuomivaara, Sami T. and Himmel, Michael E. and Moremen, Kelley W. and York, William S. and Crowley, Michael F.},
abstractNote = {Summary The mechanistic underpinnings of the complex process of plant polysaccharide biosynthesis are poorly understood, largely because of the resistance of glycosyltransferase (GT) enzymes to structural characterization. In Arabidopsis thaliana, a glycosyl transferase family 37 (GT37) fucosyltransferase 1 ( At FUT1) catalyzes the regiospecific transfer of terminal 1,2‐fucosyl residues to xyloglucan side chains – a key step in the biosynthesis of fucosylated sidechains of galactoxyloglucan. We unravel the mechanistic basis for fucosylation by At FUT1 with a multipronged approach involving protein expression, X‐ray crystallography, mutagenesis experiments and molecular simulations. Mammalian cell culture expressions enable the sufficient production of the enzyme for X‐ray crystallography, which reveals the structural architecture of At FUT1 in complex with bound donor and acceptor substrate analogs. The lack of an appropriately positioned active site residue as a catalytic base leads us to propose an atypical water‐mediated fucosylation mechanism facilitated by an H‐bonded network, which is corroborated by mutagenesis experiments as well as detailed atomistic simulations.},
doi = {10.1111/tpj.13628},
journal = {The Plant Journal},
number = 6,
volume = 91,
place = {United States},
year = {Mon Jul 03 00:00:00 EDT 2017},
month = {Mon Jul 03 00:00:00 EDT 2017}
}

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