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Title: Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases

Abstract

Summary The xyloglucan endotransglycosylase/hydrolase ( XTH ) gene family encodes enzymes of central importance to plant cell wall remodeling. The evolutionary history of plant XTH gene products is incompletely understood vis‐à‐vis the larger body of bacterial endoglycanases in Glycoside Hydrolase Family 16 ( GH 16). To provide molecular insight into this issue, high‐resolution X‐ray crystal structures and detailed enzyme kinetics of an extant transitional plant endoglucanase ( EG ) were determined. Functionally intermediate between plant XTH gene products and bacterial licheninases of GH 16, Vitis vinifera EG 16 (Vv EG 16) effectively catalyzes the hydrolysis of the backbones of two dominant plant cell wall matrix glycans, xyloglucan (XyG) and β(1,3)/β(1,4)‐mixed‐linkage glucan ( MLG ). Crystallographic complexes with extended oligosaccharide substrates reveal the structural basis for the accommodation of both unbranched, mixed‐linked ( MLG ) and highly decorated, linear (XyG) polysaccharide chains in a broad, extended active‐site cleft. Structural comparison with representative bacterial licheninases, a xyloglucan endotranglycosylase ( XET ), and a xyloglucan endohydrolase ( XEH ) outline the functional ramifications of key sequence deletions and insertions across the phylogenetic landscape of GH 16. Although the biological role(s) of EG 16 orthologs remains to be fully resolved, the present biochemical andmore » tertiary structural characterization provides key insight into plant cell wall enzyme evolution, which will continue to inform genomic analyses and functional studies across species.« less

Authors:
 [1];  [1];  [2];  [2];  [3]
  1. Michael Smith Laboratories University of British Columbia 2185 East Mall Vancouver BC V6T 1Z4 Canada, Department of Chemistry University of British Columbia 2036 Main Mall Vancouver BC V6T 1Z1 Canada
  2. Department of Biochemistry and Molecular Biology University of British Columbia 2350 Health Sciences Mall Vancouver BC V6T 1Z3 Canada
  3. Michael Smith Laboratories University of British Columbia 2185 East Mall Vancouver BC V6T 1Z4 Canada, Department of Chemistry University of British Columbia 2036 Main Mall Vancouver BC V6T 1Z1 Canada, Department of Biochemistry and Molecular Biology University of British Columbia 2350 Health Sciences Mall Vancouver BC V6T 1Z3 Canada, Department of Botany University of British Columbia 6270 University Boulevard Vancouver BC V6T 1Z4 Canada
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1401723
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 89 Journal Issue: 4; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

McGregor, Nicholas, Yin, Victor, Tung, Ching‐Chieh, Van Petegem, Filip, and Brumer, Harry. Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases. United Kingdom: N. p., 2017. Web. doi:10.1111/tpj.13421.
McGregor, Nicholas, Yin, Victor, Tung, Ching‐Chieh, Van Petegem, Filip, & Brumer, Harry. Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases. United Kingdom. https://doi.org/10.1111/tpj.13421
McGregor, Nicholas, Yin, Victor, Tung, Ching‐Chieh, Van Petegem, Filip, and Brumer, Harry. Sat . "Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases". United Kingdom. https://doi.org/10.1111/tpj.13421.
@article{osti_1401723,
title = {Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases},
author = {McGregor, Nicholas and Yin, Victor and Tung, Ching‐Chieh and Van Petegem, Filip and Brumer, Harry},
abstractNote = {Summary The xyloglucan endotransglycosylase/hydrolase ( XTH ) gene family encodes enzymes of central importance to plant cell wall remodeling. The evolutionary history of plant XTH gene products is incompletely understood vis‐à‐vis the larger body of bacterial endoglycanases in Glycoside Hydrolase Family 16 ( GH 16). To provide molecular insight into this issue, high‐resolution X‐ray crystal structures and detailed enzyme kinetics of an extant transitional plant endoglucanase ( EG ) were determined. Functionally intermediate between plant XTH gene products and bacterial licheninases of GH 16, Vitis vinifera EG 16 (Vv EG 16) effectively catalyzes the hydrolysis of the backbones of two dominant plant cell wall matrix glycans, xyloglucan (XyG) and β(1,3)/β(1,4)‐mixed‐linkage glucan ( MLG ). Crystallographic complexes with extended oligosaccharide substrates reveal the structural basis for the accommodation of both unbranched, mixed‐linked ( MLG ) and highly decorated, linear (XyG) polysaccharide chains in a broad, extended active‐site cleft. Structural comparison with representative bacterial licheninases, a xyloglucan endotranglycosylase ( XET ), and a xyloglucan endohydrolase ( XEH ) outline the functional ramifications of key sequence deletions and insertions across the phylogenetic landscape of GH 16. Although the biological role(s) of EG 16 orthologs remains to be fully resolved, the present biochemical and tertiary structural characterization provides key insight into plant cell wall enzyme evolution, which will continue to inform genomic analyses and functional studies across species.},
doi = {10.1111/tpj.13421},
journal = {The Plant Journal},
number = 4,
volume = 89,
place = {United Kingdom},
year = {Sat Feb 11 00:00:00 EST 2017},
month = {Sat Feb 11 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1111/tpj.13421

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