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Title: A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex

Abstract

Homogalacturonan (HG) is a pectic glycan in the plant cell wall that contributes to plant growth and development and cell wall structure and function, and interacts with other glycans and proteoglycans in the wall. HG is synthesized by the galacturonosyltransferase (GAUT) gene family. Two members of this family, GAUT1 and GAUT7, form a heteromeric enzyme complex in Arabidopsis thaliana. Here, we established a heterologous GAUT expression system in HEK293 cells and show that co-expression of recombinant GAUT1 with GAUT7 results in the production of a soluble GAUT1:GAUT7 complex that catalyzes elongation of HG products in vitro. The reaction rates, progress curves, and product distributions exhibited major differences dependent upon small changes in the degree of polymerization (DP) of the oligosaccharide acceptor. GAUT1:GAUT7 displayed >45-fold increased catalytic efficiency with DP11 acceptors relative to DP7 acceptors. Although GAUT1:GAUT7 synthesized high-molecular-weight polymeric HG (>100 kDa) in a substrate concentration–dependent manner typical of distributive (nonprocessive) glycosyltransferases with DP11 acceptors, reactions primed with short-chain acceptors resulted in a bimodal product distribution of glycan products that has previously been reported as evidence for a processive model of GT elongation. As an alternative to the processive glycosyltransfer model, a two-phase distributive elongation model is proposed in whichmore » a slow phase, which includes the de novo initiation of HG and elongation of short-chain acceptors, is distinguished from a phase of rapid elongation of intermediate- and long-chain acceptors. Upon reaching a critical chain length of DP11, GAUT1:GAUT7 elongates HG to high-molecular-weight products.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  2. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Mascoma LLC (Lallemand Inc.), Lebanon, NH (United States)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1611056
Grant/Contract Number:  
SC0008472; FG02-93ER20097; FG02-12ER16324; DBI-0421683; PS02-06ER64304; 2010-65115-20396; P41GM103390; P01GM107012.
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 293; Journal Issue: 49; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Biochemistry & Molecular Biology; plant cell wall; glycosyltransferase; protein complex; enzyme mechanism; processivity; homogalacturonan; pectin; pectic glycan; galacturonosyltransferase; polygalacturonide transferase

Citation Formats

Amos, Robert A., Pattathil, Sivakumar, Yang, Jeong-Yeh, Atmodjo, Melani A., Urbanowicz, Breeanna R., Moremen, Kelley W., and Mohnen, Debra. A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex. United States: N. p., 2018. Web. doi:10.1074/jbc.ra118.004463.
Amos, Robert A., Pattathil, Sivakumar, Yang, Jeong-Yeh, Atmodjo, Melani A., Urbanowicz, Breeanna R., Moremen, Kelley W., & Mohnen, Debra. A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex. United States. doi:10.1074/jbc.ra118.004463.
Amos, Robert A., Pattathil, Sivakumar, Yang, Jeong-Yeh, Atmodjo, Melani A., Urbanowicz, Breeanna R., Moremen, Kelley W., and Mohnen, Debra. Tue . "A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex". United States. doi:10.1074/jbc.ra118.004463. https://www.osti.gov/servlets/purl/1611056.
@article{osti_1611056,
title = {A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex},
author = {Amos, Robert A. and Pattathil, Sivakumar and Yang, Jeong-Yeh and Atmodjo, Melani A. and Urbanowicz, Breeanna R. and Moremen, Kelley W. and Mohnen, Debra},
abstractNote = {Homogalacturonan (HG) is a pectic glycan in the plant cell wall that contributes to plant growth and development and cell wall structure and function, and interacts with other glycans and proteoglycans in the wall. HG is synthesized by the galacturonosyltransferase (GAUT) gene family. Two members of this family, GAUT1 and GAUT7, form a heteromeric enzyme complex in Arabidopsis thaliana. Here, we established a heterologous GAUT expression system in HEK293 cells and show that co-expression of recombinant GAUT1 with GAUT7 results in the production of a soluble GAUT1:GAUT7 complex that catalyzes elongation of HG products in vitro. The reaction rates, progress curves, and product distributions exhibited major differences dependent upon small changes in the degree of polymerization (DP) of the oligosaccharide acceptor. GAUT1:GAUT7 displayed >45-fold increased catalytic efficiency with DP11 acceptors relative to DP7 acceptors. Although GAUT1:GAUT7 synthesized high-molecular-weight polymeric HG (>100 kDa) in a substrate concentration–dependent manner typical of distributive (nonprocessive) glycosyltransferases with DP11 acceptors, reactions primed with short-chain acceptors resulted in a bimodal product distribution of glycan products that has previously been reported as evidence for a processive model of GT elongation. As an alternative to the processive glycosyltransfer model, a two-phase distributive elongation model is proposed in which a slow phase, which includes the de novo initiation of HG and elongation of short-chain acceptors, is distinguished from a phase of rapid elongation of intermediate- and long-chain acceptors. Upon reaching a critical chain length of DP11, GAUT1:GAUT7 elongates HG to high-molecular-weight products.},
doi = {10.1074/jbc.ra118.004463},
journal = {Journal of Biological Chemistry},
issn = {0021-9258},
number = 49,
volume = 293,
place = {United States},
year = {2018},
month = {10}
}

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