Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis
Abstract
Arabinogalactan-proteins (AGPs) are highly glycosylated hydroxyproline-rich glycoproteins present in plant cell walls. AGPs are characterized by arabinose-/galactose-rich side chains, which define their interactive molecular surface. Fucose residues are found in some dicotyledon AGPs, and AGP fucosylation is developmentally regulated. We previously identified Arabidopsis thaliana FUT4 and FUT6 genes as AGP-specific fucosyltransferases (FUTs) based on their enzymatic activities when heterologously expressed in tobacco (Nicotiana tabacum) BY2 suspension-cultured cells. Here, the functions of FUT4 and FUT6 and the physiological roles of fucosylated AGPs were further investigated using Arabidopsis fut4, fut6, and fut4/fut6 mutant plants. All mutant plants showed no phenotypic differences compared to wild-type plants under physiological conditions, but showed reduced root growth in the presence of elevated NaCl. However, roots of wild-type and fut4 mutant plants contained terminal fucose epitopes, which were absent in fut6 and fut4/fut6 mutant plants as indicated by eel lectin staining. Monosaccharide analysis showed fucose was present in wild-type leaf and root AGPs, but absent in fut4 leaf AGPs and in fut4/fut6 double mutant leaf and root AGPs, indicating that FUT4 was required for fucosylation of leaf AGPs while both FUT4 and FUT6 contributed to fucosylation of root AGPs. Glycome profiling of cell wall fractions from mutantmore »
- Authors:
-
- Ohio Univ., Athens, OH (United States). Dept. of Environmental and Plant Biology; Ohio Univ., Athens, OH (United States). Molecular and Cellular Biology Program; Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)
- Ohio Univ., Athens, OH (United States). Dept. of Environmental and Plant Biology; Ohio Univ., Athens, OH (United States). Molecular and Cellular Biology Program
- Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
- Ohio Univ., Athens, OH (United States). Dept. of Environmental and Plant Biology
- SAS Inst., Cary, NC (United States)
- Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Univ. of Georgia, Athens, GA (United States). Dept. of Plant Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; USDA; National Science Foundation (NSF)
- OSTI Identifier:
- 1625382
- Grant/Contract Number:
- AC02-05CH11231; PS02-06ER64304; 2008-35318-04563; 2008-35318-04572; DBI-0421683
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Experimental Botany
- Additional Journal Information:
- Journal Volume: 64; Journal Issue: 18; Journal ID: ISSN 0022-0957
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; plant sciences; arabidopsis; arabinogalactan-proteins; fucosyltransferase; glycosylation; hydroxyproline-rich proteins; plant cell wall
Citation Formats
Liang, Yan, Basu, Debarati, Pattathil, Sivakumar, Xu, Wen-liang, Venetos, Alexandra, Martin, Stanton L., Faik, Ahmed, Hahn, Michael G., and Showalter, Allan M. Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis. United States: N. p., 2013.
Web. doi:10.1093/jxb/ert321.
Liang, Yan, Basu, Debarati, Pattathil, Sivakumar, Xu, Wen-liang, Venetos, Alexandra, Martin, Stanton L., Faik, Ahmed, Hahn, Michael G., & Showalter, Allan M. Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis. United States. https://doi.org/10.1093/jxb/ert321
Liang, Yan, Basu, Debarati, Pattathil, Sivakumar, Xu, Wen-liang, Venetos, Alexandra, Martin, Stanton L., Faik, Ahmed, Hahn, Michael G., and Showalter, Allan M. Mon .
"Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis". United States. https://doi.org/10.1093/jxb/ert321. https://www.osti.gov/servlets/purl/1625382.
@article{osti_1625382,
title = {Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis},
author = {Liang, Yan and Basu, Debarati and Pattathil, Sivakumar and Xu, Wen-liang and Venetos, Alexandra and Martin, Stanton L. and Faik, Ahmed and Hahn, Michael G. and Showalter, Allan M.},
abstractNote = {Arabinogalactan-proteins (AGPs) are highly glycosylated hydroxyproline-rich glycoproteins present in plant cell walls. AGPs are characterized by arabinose-/galactose-rich side chains, which define their interactive molecular surface. Fucose residues are found in some dicotyledon AGPs, and AGP fucosylation is developmentally regulated. We previously identified Arabidopsis thaliana FUT4 and FUT6 genes as AGP-specific fucosyltransferases (FUTs) based on their enzymatic activities when heterologously expressed in tobacco (Nicotiana tabacum) BY2 suspension-cultured cells. Here, the functions of FUT4 and FUT6 and the physiological roles of fucosylated AGPs were further investigated using Arabidopsis fut4, fut6, and fut4/fut6 mutant plants. All mutant plants showed no phenotypic differences compared to wild-type plants under physiological conditions, but showed reduced root growth in the presence of elevated NaCl. However, roots of wild-type and fut4 mutant plants contained terminal fucose epitopes, which were absent in fut6 and fut4/fut6 mutant plants as indicated by eel lectin staining. Monosaccharide analysis showed fucose was present in wild-type leaf and root AGPs, but absent in fut4 leaf AGPs and in fut4/fut6 double mutant leaf and root AGPs, indicating that FUT4 was required for fucosylation of leaf AGPs while both FUT4 and FUT6 contributed to fucosylation of root AGPs. Glycome profiling of cell wall fractions from mutant roots and leaves showed distinct glycome profiles compared to wild-type plants, indicating that fucosyl residues on AGPs may regulate intermolecular interactions between AGPs and other wall components. The current work exemplifies the possibilities of refinement of cell wall structures by manipulation of a single or a few cell wall biosynthetic genes.},
doi = {10.1093/jxb/ert321},
journal = {Journal of Experimental Botany},
number = 18,
volume = 64,
place = {United States},
year = {Mon Oct 14 00:00:00 EDT 2013},
month = {Mon Oct 14 00:00:00 EDT 2013}
}
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Control of stem-cell niche establishment in Arabidopsis flowers by REVOLUTA and the LEAFY-RAX1 module
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- Grégoire, Denay; Gabrielle, Tichtinsky; Marie, Le Masson
- Semantic Scholar
A cell surface arabinogalactan-peptide influences root hair cell fate
journal, November 2019
- Borassi, Cecilia; Gloazzo, JAvier; Ricardi, Martiniano M.
- New Phytologist
A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis
journal, December 2015
- Basu, Debarati; Tian, Lu; Wang, Wuda
- BMC Plant Biology, Vol. 15, Issue 1
Two Hydroxyproline Galactosyltransferases, GALT5 and GALT2, Function in Arabinogalactan-Protein Glycosylation, Growth and Development in Arabidopsis
journal, May 2015
- Basu, Debarati; Wang, Wuda; Ma, Siyi
- PLOS ONE, Vol. 10, Issue 5
Post-Synthetic Defucosylation of AGP by Aspergillus nidulans α-1,2-Fucosidase Expressed in Arabidopsis Apoplast Induces Compensatory Upregulation of α-1,2-Fucosyltransferases
journal, July 2016
- Pogorelko, Gennady V.; Reem, Nathan T.; Young, Zachary T.
- PLOS ONE, Vol. 11, Issue 7
Characterisation of FUT4 and FUT6 α-(1 → 2)-fucosyltransferases reveals that absence of root arabinogalactan fucosylation increases Arabidopsis root growth salt sensitivity.
text, January 2014
- Tryfona, Theodora; Theys, Tina E.; Wagner, Tanya
- Apollo - University of Cambridge Repository
Immunological Approaches to Biomass Characterization and Utilization
journal, October 2015
- Pattathil, Sivakumar; Avci, Utku; Zhang, Tiantian
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function
journal, October 2014
- Nguema-Ona, Eric; Vicré-Gibouin, Maïté; Gotté, Maxime
- Frontiers in Plant Science, Vol. 5
Extensin and Arabinogalactan-Protein Biosynthesis: Glycosyltransferases, Research Challenges, and Biosensors
journal, June 2016
- Showalter, Allan M.; Basu, Debarati
- Frontiers in Plant Science, Vol. 7
Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability
journal, June 2016
- Pattathil, Sivakumar; Ingwers, Miles W.; Victoriano, Olivia L.
- Frontiers in Plant Science, Vol. 7