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Title: Suppression of Arabidopsis GGLT 1 affects growth by reducing the L‐galactose content and borate cross‐linking of rhamnogalacturonan‐ II

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.14088· OSTI ID:1478429
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  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

Summary 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 ( GONST 3/ GGLT 1) has been reduced. In the GGLT 1 ‐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, GGLT 1 ‐silenced plants display a loss of cell wall integrity under salt stress. We conclude that GGLT 1 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
DE‐FG02‐96ER20220; AC02-05CH11231
OSTI ID:
1478429
Alternate ID(s):
OSTI ID: 1478430; OSTI ID: 1506359
Journal Information:
The Plant Journal, Journal Name: The Plant Journal Vol. 96 Journal Issue: 5; ISSN 0960-7412
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 24 works
Citation information provided by
Web of Science

References (70)

Generation of a monoclonal antibody specific to (1→5)-α-l-arabinan journal March 1998
Identification and Characterization of GONST1, a Golgi-Localized GDP-Mannose Transporter in Arabidopsis journal October 2001
The Minimum Open Reading Frame, AUG-Stop, Induces Boron-Dependent Ribosome Stalling and mRNA Degradation journal October 2016
Boron deficiency in woody plants: various responses and tolerance mechanisms journal October 2015
The Arabidopsis Golgi-localized GDP-L-fucose transporter is required for plant development journal July 2016
Structural characterization of novel l-galactose-containing oligosaccharide subunits of jojoba seed xyloglucans journal October 1997
The plant glycosyltransferase clone collection for functional genomics journal July 2014
Silencing of the GDP-d-mannose 3,5-Epimerase Affects the Structure and Cross-linking of the Pectic Polysaccharide Rhamnogalacturonan II and Plant Growth in Tomato journal January 2011
A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies journal April 2010
Symbol Nomenclature for Graphical Representations of Glycans journal November 2015
Boron deficiency and transcript level changes journal August 2011
Rapid Structural Phenotyping of Plant Cell Wall Mutants by Enzymatic Oligosaccharide Fingerprinting journal December 2002
The biosynthesis of the branched-chain sugar d-apiose in plants: functional cloning and characterization of a UDP-d-apiose/UDP-d-xylose synthase from Arabidopsis journal September 2003
Occurrence of the Primary Cell Wall Polysaccharide Rhamnogalacturonan II in Pteridophytes, Lycophytes, and Bryophytes. Implications for the Evolution of Vascular Plants journal December 2003
The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose journal March 1997
Cell wall integrity signaling in plants: “To grow or not to grow that's the question” journal March 2016
Root cell wall solutions for crop plants in saline soils journal April 2018
Arabidopsis thaliana RGXT1 and RGXT2 Encode Golgi-Localized (1,3)-α-d-Xylosyltransferases Involved in the Synthesis of Pectic Rhamnogalacturonan-II journal October 2006
Ascorbate biosynthesis and function in photoprotection journal October 2000
Two genes in Arabidopsis thaliana encoding GDP-l-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability: Role of GDP-l-Gal phosphorylase in ascorbate biosynthesis journal September 2007
Rhamnogalacturonan II structure shows variation in the side chains monosaccharide composition and methylation status within and across different plant species journal July 2013
Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes journal May 2003
Localization of Pectic Galactan in Tomato Cell Walls Using a Monoclonal Antibody Specific to (1[->]4)-[beta]-D-Galactan journal April 1997
Xyloglucan−pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall journal November 2007
Boron in plants and animals: Is there a role beyond cell-wall structure? journal February 2007
ARABINAN DEFICIENT 1 Is a Putative Arabinosyltransferase Involved in Biosynthesis of Pectic Arabinan in Arabidopsis journal December 2005
MALE GAMETOPHYTE DEFECTIVE 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis: MGP4 is required for pollen tube growth journal December 2010
Two Chains of Rhamnogalacturonan II Are Cross-Linked by Borate-Diol Ester Bonds in Higher Plant Cell Walls journal March 1996
RHAMNOGALACTURONAN II: Structure and Function of a Borate Cross-Linked Cell Wall Pectic Polysaccharide journal June 2004
Functional characterisation of a putative rhamnogalacturonan II specific xylosyltransferase journal August 2008
A putative Arabidopsis thaliana glycosyltransferase, At4g01220, which is closely related to three plant cell wall-specific xylosyltransferases, is differentially expressed spatially and temporally journal March 2011
Rhamnogalacturonan-II, a Pectic Polysaccharide in the Walls of Growing Plant Cell, Forms a Dimer That Is Covalently Cross-linked by a Borate Ester journal September 1996
Boron in Plants: Deficiency and Toxicity journal October 2008
Modification of Epidermal Growth Factor-like Repeats with O- Fucose : MOLECULAR CLONING AND EXPRESSION OF A NOVEL GDP-FUCOSE PROTEIN journal August 2001
Preparing rhamnogalacturonan II domains from seven plant pectins using Penicillium oxalicum degradation and their structural comparison journal January 2018
Glycosylinositol phosphorylceramides from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan II journal June 2014
The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA journal February 2017
Deficiency and toxicity of boron: Alterations in growth, oxidative damage and uptake by citrange orange plants journal November 2017
Arabidopsis mannan synthase CSLA9 and glucan synthase CSLC4 have opposite orientations in the Golgi membrane: Hemicellulosic glycan synthase topology journal November 2010
Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis journal November 2016
Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis journal September 2005
The synthesis of the rhamnogalacturonan II component 3-deoxy-D-manno-2-octulosonic acid (Kdo) is required for pollen tube growth and elongation journal July 2008
Synthesis of borate cross-linked rhamnogalacturonan II journal April 2015
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar journal March 1959
Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR journal December 2016
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance journal November 2008
Enhancement of the Quality of MALDI Mass Spectra of Highly Acidic Oligosaccharides by Using a Nafion-Coated Probe journal February 2001
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures journal July 1962
The Pore Size of Non-Graminaceous Plant Cell Walls Is Rapidly Decreased by Borate Ester Cross-Linking of the Pectic Polysaccharide Rhamnogalacturonan II journal November 1999
Complex pectin metabolism by gut bacteria reveals novel catalytic functions journal March 2017
Assay and heterologous expression in Pichia pastoris of plant cell wall type-II membrane anchored glycosyltransferases journal May 2009
Altered Growth and Cell Walls in a Fucose-Deficient Mutant of Arabidopsis journal August 1993
An Arabidopsis Cell Wall Proteoglycan Consists of Pectin and Arabinoxylan Covalently Linked to an Arabinogalactan Protein journal January 2013
Glycan complexity dictates microbial resource allocation in the large intestine journal June 2015
Evolving Views of Pectin Biosynthesis journal April 2013
Arabidopsis thaliana expresses multiple Golgi-localised nucleotide-sugar transporters related to GONST1 journal October 2004
Requirement of Borate Cross-Linking of Cell Wall Rhamnogalacturonan II for Arabidopsis Growth journal October 2001
Abnormal Glycosphingolipid Mannosylation Triggers Salicylic Acid–Mediated Responses in Arabidopsis journal May 2013
Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls journal March 1998
An extended set of monoclonal antibodies to pectic homogalacturonan journal September 2009
Plant Nucleotide Sugar Formation, Interconversion, and Salvage by Sugar Recycling* journal June 2011
[2-3H]Mannose Incorporation in Cultured Plant Cells: Investigation of L-Galactose Residues of the Primary Cell Wall journal May 1988
The Gene Expression and Enzyme Activity of Plant 3-Deoxy-D-Manno-2-Octulosonic Acid-8-Phosphate Synthase Are Preferentially Associated with Cell Division in a Cell Cycle-Dependent Manner journal August 2003
Two tomato GDP-D-mannose epimerase isoforms involved in ascorbate biosynthesis play specific roles in cell wall biosynthesis and development journal July 2016
Depletion of UDP-d-apiose/UDP-d-xylose Synthases Results in Rhamnogalacturonan-II Deficiency, Cell Wall Thickening, and Cell Death in Higher Plants journal March 2006
GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato journal November 2009
The Golgi localized bifunctional UDP-rhamnose/UDP-galactose transporter family of Arabidopsis journal July 2014
Changes in the abundance of cell wall apiogalacturonan and xylogalacturonan and conservation of rhamnogalacturonan II structure during the diversification of the Lemnoideae journal December 2017
Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion journal January 2014