Structural and biochemical insight into a modular β-1,4-galactan synthase in plants
Abstract
Rhamnogalacturonan I (RGI) is a structurally complex pectic polysaccharide with a backbone of alternating rhamnose and galacturonic acid residues substituted with arabinan and galactan side chains. Galactan synthase 1 (GalS1) transfers galactose and arabinose to either extend or cap the ..beta..-1,4-galactan side chains of RGI, respectively. Here we report the structure of GalS1 from Populus trichocarpa, showing a modular protein consisting of an N-terminal domain that represents the founding member of a new family of carbohydrate-binding module, CBM95, and a C-terminal glycosyltransferase family 92 (GT92) catalytic domain that adopts a GT-A fold. GalS1 exists as a dimer in vitro, with stem domains interacting across the chains in a 'handshake' orientation that is essential for maintaining stability and activity. In addition to understanding the enzymatic mechanism of GalS1, here we gained insight into the donor and acceptor substrate binding sites using deep evolutionary analysis, molecular simulations and biochemical studies. Combining all the results, a mechanism for GalS1 catalysis and a new model for pectic galactan side-chain addition are proposed.
- Authors:
-
- University of Georgia, Athens, GA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Joint BioEnergy Institute and Environmental Genomics and Systems Biology Division
- University of Georgia, Athens, GA (United States)
- National Renewable Energy Laboratory (NREL), Golden, CO (United States). Renewable Resources and Enabling Science Center
- University of Georgia, Athens, GA (United States); National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Joint BioEnergy Institute and Environmental Genomics and Systems Biology Division; University of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Howard Hughes Medical Institute; National Institutes of Health (NIH)
- OSTI Identifier:
- 1962035
- Report Number(s):
- NREL/JA-2800-84906
Journal ID: ISSN 2055-0278; MainId:85679;UUID:4aee18d7-6dd5-42f3-8a72-27f01c7e554a;MainAdminID:69034
- Grant/Contract Number:
- AC36-08GO28308; AC02-05CH11231; P30 GM124169; R35 GM139656; R01 GM130915; P41GM103390
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Plants (Online)
- Additional Journal Information:
- Journal Name: Nature Plants (Online); Journal Volume: 9; Journal Issue: 3; Journal ID: ISSN 2055-0278
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; docking; galactosyl transferase; molecular dynamics; Rhamnogalacturonan-I; x-ray crystallography
Citation Formats
Prabhakar, Pradeep Kumar, Pereira, Jose Henrique, Taujale, Rahil, Shao, Wanchen, Bharadwaj, Vivek S., Chapla, Digantkumar, Yang, Jeong-Yeh, Bomble, Yannick J., Moremen, Kelley W., Kannan, Natarajan, Hammel, Michal, Adams, Paul D., Scheller, Henrik V., and Urbanowicz, Breeanna R. Structural and biochemical insight into a modular β-1,4-galactan synthase in plants. United States: N. p., 2023.
Web. doi:10.1038/s41477-023-01358-4.
Prabhakar, Pradeep Kumar, Pereira, Jose Henrique, Taujale, Rahil, Shao, Wanchen, Bharadwaj, Vivek S., Chapla, Digantkumar, Yang, Jeong-Yeh, Bomble, Yannick J., Moremen, Kelley W., Kannan, Natarajan, Hammel, Michal, Adams, Paul D., Scheller, Henrik V., & Urbanowicz, Breeanna R. Structural and biochemical insight into a modular β-1,4-galactan synthase in plants. United States. https://doi.org/10.1038/s41477-023-01358-4
Prabhakar, Pradeep Kumar, Pereira, Jose Henrique, Taujale, Rahil, Shao, Wanchen, Bharadwaj, Vivek S., Chapla, Digantkumar, Yang, Jeong-Yeh, Bomble, Yannick J., Moremen, Kelley W., Kannan, Natarajan, Hammel, Michal, Adams, Paul D., Scheller, Henrik V., and Urbanowicz, Breeanna R. Mon .
"Structural and biochemical insight into a modular β-1,4-galactan synthase in plants". United States. https://doi.org/10.1038/s41477-023-01358-4. https://www.osti.gov/servlets/purl/1962035.
@article{osti_1962035,
title = {Structural and biochemical insight into a modular β-1,4-galactan synthase in plants},
author = {Prabhakar, Pradeep Kumar and Pereira, Jose Henrique and Taujale, Rahil and Shao, Wanchen and Bharadwaj, Vivek S. and Chapla, Digantkumar and Yang, Jeong-Yeh and Bomble, Yannick J. and Moremen, Kelley W. and Kannan, Natarajan and Hammel, Michal and Adams, Paul D. and Scheller, Henrik V. and Urbanowicz, Breeanna R.},
abstractNote = {Rhamnogalacturonan I (RGI) is a structurally complex pectic polysaccharide with a backbone of alternating rhamnose and galacturonic acid residues substituted with arabinan and galactan side chains. Galactan synthase 1 (GalS1) transfers galactose and arabinose to either extend or cap the ..beta..-1,4-galactan side chains of RGI, respectively. Here we report the structure of GalS1 from Populus trichocarpa, showing a modular protein consisting of an N-terminal domain that represents the founding member of a new family of carbohydrate-binding module, CBM95, and a C-terminal glycosyltransferase family 92 (GT92) catalytic domain that adopts a GT-A fold. GalS1 exists as a dimer in vitro, with stem domains interacting across the chains in a 'handshake' orientation that is essential for maintaining stability and activity. In addition to understanding the enzymatic mechanism of GalS1, here we gained insight into the donor and acceptor substrate binding sites using deep evolutionary analysis, molecular simulations and biochemical studies. Combining all the results, a mechanism for GalS1 catalysis and a new model for pectic galactan side-chain addition are proposed.},
doi = {10.1038/s41477-023-01358-4},
journal = {Nature Plants (Online)},
number = 3,
volume = 9,
place = {United States},
year = {Mon Feb 27 00:00:00 EST 2023},
month = {Mon Feb 27 00:00:00 EST 2023}
}
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