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Title: Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II

Abstract

Boron is a micronutrient that is required for the normal growth and development of vascular plants, but its precise functions remain a subject of debate. One established role for boron is in the cell wall where it forms a diester cross-link between two monomers of the low-abundance pectic polysaccharide rhamnogalacturonan-II (RG-II). The inability of RG-II to properly assemble into a dimer results in the formation of cell walls with abnormal biochemical and biomechanical properties and has a severe impact on plant productivity. Here we describe the effects on RG-II structure and cross-linking and on the growth of plants in which the expression of a GDP-sugar transporter (GONST3/GGLT1) has been reduced. In the GGLT1-silenced plants the amount of L-galactose in side-chain A of RG-II is reduced by up to 50%. This leads to a reduction in the extent of RG-II cross-linking in the cell walls as well as a reduction in the stability of the dimer in the presence of calcium chelators. The silenced plants have a dwarf phenotype, which is rescued by growth in the presence of increased amounts of boric acid. Similar to the mur1 mutant, which also disrupts RG-II cross-linking, GGLT1-silenced plants display a loss of cell wallmore » integrity under salt stress. We conclude that GGLT1 is probably the primary Golgi GDP-L-galactose transporter, and provides GDP-L-galactose for RG-II biosynthesis. We propose that the L-galactose residue is critical for RG-II dimerization and for the stability of the borate cross-link.« less

Authors:
 [1];  [1];  [2];  [2];  [3];  [4];  [1];  [1];  [4];  [5];  [2]; ORCiD logo [1]
  1. Joint BioEnergy Institute, Emeryville CA 94608 USA, Biosciences Area, Lawrence Berkeley National Laboratory, Berkeley CA 94720 USA
  2. Complex Carbohydrate Research Center, The University of Georgia, Athens GA 30602 USA
  3. Department of Plant Biology, Carnegie Institute for Science, Stanford CA 94305 USA
  4. Graduate School of Science and Engineering, Saitama University, Saitama 338-8570 Japan
  5. Department of Plant Biology, Carnegie Institute for Science, Stanford CA 94305 USA, Department of Biology, Stanford University, Stanford CA 94305 USA
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1478429
Alternate Identifier(s):
OSTI ID: 1478430; OSTI ID: 1506359
Grant/Contract Number:  
FG02-96ER20220; AC02-05CH11231
Resource Type:
Journal Article: Published Article
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 96 Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; boron; golgi; nucleotide‐sugar transporter; pectin; rhamnogalacturonan II

Citation Formats

Sechet, Julien, Htwe, Soe, Urbanowicz, Breeanna, Agyeman, Abigail, Feng, Wei, Ishikawa, Toshiki, Colomes, Marianne, Kumar, Kavitha Satish, Kawai-Yamada, Maki, Dinneny, José R., O'Neill, Malcolm A., and Mortimer, Jenny C. Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II. United Kingdom: N. p., 2018. Web. doi:10.1111/tpj.14088.
Sechet, Julien, Htwe, Soe, Urbanowicz, Breeanna, Agyeman, Abigail, Feng, Wei, Ishikawa, Toshiki, Colomes, Marianne, Kumar, Kavitha Satish, Kawai-Yamada, Maki, Dinneny, José R., O'Neill, Malcolm A., & Mortimer, Jenny C. Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II. United Kingdom. doi:10.1111/tpj.14088.
Sechet, Julien, Htwe, Soe, Urbanowicz, Breeanna, Agyeman, Abigail, Feng, Wei, Ishikawa, Toshiki, Colomes, Marianne, Kumar, Kavitha Satish, Kawai-Yamada, Maki, Dinneny, José R., O'Neill, Malcolm A., and Mortimer, Jenny C. Sat . "Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II". United Kingdom. doi:10.1111/tpj.14088.
@article{osti_1478429,
title = {Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II},
author = {Sechet, Julien and Htwe, Soe and Urbanowicz, Breeanna and Agyeman, Abigail and Feng, Wei and Ishikawa, Toshiki and Colomes, Marianne and Kumar, Kavitha Satish and Kawai-Yamada, Maki and Dinneny, José R. and O'Neill, Malcolm A. and Mortimer, Jenny C.},
abstractNote = {Boron is a micronutrient that is required for the normal growth and development of vascular plants, but its precise functions remain a subject of debate. One established role for boron is in the cell wall where it forms a diester cross-link between two monomers of the low-abundance pectic polysaccharide rhamnogalacturonan-II (RG-II). The inability of RG-II to properly assemble into a dimer results in the formation of cell walls with abnormal biochemical and biomechanical properties and has a severe impact on plant productivity. Here we describe the effects on RG-II structure and cross-linking and on the growth of plants in which the expression of a GDP-sugar transporter (GONST3/GGLT1) has been reduced. In the GGLT1-silenced plants the amount of L-galactose in side-chain A of RG-II is reduced by up to 50%. This leads to a reduction in the extent of RG-II cross-linking in the cell walls as well as a reduction in the stability of the dimer in the presence of calcium chelators. The silenced plants have a dwarf phenotype, which is rescued by growth in the presence of increased amounts of boric acid. Similar to the mur1 mutant, which also disrupts RG-II cross-linking, GGLT1-silenced plants display a loss of cell wall integrity under salt stress. We conclude that GGLT1 is probably the primary Golgi GDP-L-galactose transporter, and provides GDP-L-galactose for RG-II biosynthesis. We propose that the L-galactose residue is critical for RG-II dimerization and for the stability of the borate cross-link.},
doi = {10.1111/tpj.14088},
journal = {The Plant Journal},
issn = {0960-7412},
number = 5,
volume = 96,
place = {United Kingdom},
year = {2018},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1111/tpj.14088

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Cited by: 7 works
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