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:
-
- Univ. of Georgia, Athens, GA (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- 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}
}
Web of Science
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