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Title: MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage

Abstract

Plants invest a lot of their resources into the production of an extracellular matrix built of polysaccharides. While the composition of the cell wall is relatively well characterized, the functions of the individual polymers and the enzymes that catalyze their biosynthesis remain poorly understood. We exploited the Arabidopsis ( Arabidopsis thaliana) seed coat epidermis (SCE) to study cell wall synthesis. SCE cells produce mucilage, a specialized secondary wall that is rich in pectin, at a precise stage of development. A coexpression search for MUCILAGE-RELATED (MUCI) genes identified MUCI10 as a key determinant of mucilage properties. MUCI10 is closely related to a fenugreek ( Trigonella foenumgraecum) enzyme that has in vitro galactomannan α-1,6-galactosyltransferase activity. Our detailed analysis of the muci10 mutants demonstrates that mucilage contains highly branched galactoglucomannan (GGM) rather than unbranched glucomannan. Muci10 likely decorates glucomannan, synthesized by CELLULOSE SYNTHASE-LIKE A2, with galactose residues in vivo. The degree of galactosylation is essential for the synthesis of the GGM backbone, the structure of cellulose, mucilage density, as well as the adherence of pectin. We propose that GGM scaffolds control mucilage architecture along with cellulosic rays and show that Arabidopsis SCE cells represent an excellent model in which to study the synthesismore » and function of GGM. Arabidopsis natural varieties with defects similar to muci10 mutants may reveal additional genes involved in GGM synthesis. Since GGM is the most abundant hemicellulose in the secondary walls of gymnosperms, understanding its biosynthesis may facilitate improvements in the production of valuable commodities from softwoods.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [2]; ORCiD logo [3];  [4];  [5];  [2];  [1];  [1]
  1. Forschungszentrum Jülich, Juelich (Germany). Inst. for Biosciences and Geosciences
  2. Inst. National de la Recherche Agronomique and AgroParisTech, Versailles (France). Inst. Jean-Pierre Bourgin, ERL Centre National de la Recherche Scientifique
  3. RWTH Aachen Univ. (Germany). Inst. for Botany and Molecular Genetics, BioEconomy Science Center
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst. and Physical Biosciences Division
  5. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst. and Physical Biosciences Division
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); Natural Sciences and Engineering Research Council of Canada (NSERC)
OSTI Identifier:
1512244
Grant/Contract Number:  
AC02-05CH11231; 313/323–400–00213
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Volume: 169; Journal Issue: 1; Journal ID: ISSN 0032-0889
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Voiniciuc, Cătălin, Schmidt, Maximilian Heinrich-Wilhelm, Berger, Adeline, Yang, Bo, Ebert, Berit, Scheller, Henrik V., North, Helen M., Usadel, Björn, and Günl, Markus. MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage. United States: N. p., 2015. Web. doi:10.1104/pp.15.00851.
Voiniciuc, Cătălin, Schmidt, Maximilian Heinrich-Wilhelm, Berger, Adeline, Yang, Bo, Ebert, Berit, Scheller, Henrik V., North, Helen M., Usadel, Björn, & Günl, Markus. MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage. United States. doi:10.1104/pp.15.00851.
Voiniciuc, Cătălin, Schmidt, Maximilian Heinrich-Wilhelm, Berger, Adeline, Yang, Bo, Ebert, Berit, Scheller, Henrik V., North, Helen M., Usadel, Björn, and Günl, Markus. Tue . "MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage". United States. doi:10.1104/pp.15.00851. https://www.osti.gov/servlets/purl/1512244.
@article{osti_1512244,
title = {MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage},
author = {Voiniciuc, Cătălin and Schmidt, Maximilian Heinrich-Wilhelm and Berger, Adeline and Yang, Bo and Ebert, Berit and Scheller, Henrik V. and North, Helen M. and Usadel, Björn and Günl, Markus},
abstractNote = {Plants invest a lot of their resources into the production of an extracellular matrix built of polysaccharides. While the composition of the cell wall is relatively well characterized, the functions of the individual polymers and the enzymes that catalyze their biosynthesis remain poorly understood. We exploited the Arabidopsis (Arabidopsis thaliana) seed coat epidermis (SCE) to study cell wall synthesis. SCE cells produce mucilage, a specialized secondary wall that is rich in pectin, at a precise stage of development. A coexpression search for MUCILAGE-RELATED (MUCI) genes identified MUCI10 as a key determinant of mucilage properties. MUCI10 is closely related to a fenugreek (Trigonella foenumgraecum) enzyme that has in vitro galactomannan α-1,6-galactosyltransferase activity. Our detailed analysis of the muci10 mutants demonstrates that mucilage contains highly branched galactoglucomannan (GGM) rather than unbranched glucomannan. Muci10 likely decorates glucomannan, synthesized by CELLULOSE SYNTHASE-LIKE A2, with galactose residues in vivo. The degree of galactosylation is essential for the synthesis of the GGM backbone, the structure of cellulose, mucilage density, as well as the adherence of pectin. We propose that GGM scaffolds control mucilage architecture along with cellulosic rays and show that Arabidopsis SCE cells represent an excellent model in which to study the synthesis and function of GGM. Arabidopsis natural varieties with defects similar to muci10 mutants may reveal additional genes involved in GGM synthesis. Since GGM is the most abundant hemicellulose in the secondary walls of gymnosperms, understanding its biosynthesis may facilitate improvements in the production of valuable commodities from softwoods.},
doi = {10.1104/pp.15.00851},
journal = {Plant Physiology (Bethesda)},
issn = {0032-0889},
number = 1,
volume = 169,
place = {United States},
year = {2015},
month = {7}
}

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Cited by: 59 works
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Figures / Tables:

Figure 1 Figure 1: Analysis of the MUCI10 gene and its paralog, GT6. A, MUCI10 is coexpressed with known mucilage genes. Microarray data were visualized with GeneMANIA using all 14 genes as baits (Warde-Farley et al., 2010). B, MUCI10 and GT6 insertions and RT-PCR amplicons (red arrows). Bars = 200 bp. Cmore » to E, RT-PCR (C) and qRT-PCR (D and E) analyses of gene expression in siliques. Two wild-type (WT) biological replicates were tested at three stages of development (heart, linear cotyledon, and mature green), while all mutants were examined at the linear cotyledon stage. D and E, MUCI10 expression (normalized to UBIQUITIN5) relative to the first wild type in each set. KNAT7 is a transcription factor predicted to promote hemicellulose biosynthesis in seed mucilage (Voiniciuc et al., 2015). Data show means + SD of four (D) or three (E) technical replicates.« less

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Works referencing / citing this record:

TRM 4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA 3
journal, September 2018

  • Yang, Bo; Voiniciuc, Cătălin; Fu, Lanbao
  • New Phytologist, Vol. 221, Issue 2
  • DOI: 10.1111/nph.15442

MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage
text, January 2015


The role of COBRA ‐ LIKE 2 function, as part of the complex network of interacting pathways regulating Arabidopsis seed mucilage polysaccharide matrix organization
journal, March 2018

  • Ben‐Tov, Daniela; Idan‐Molakandov, Anat; Hugger, Anat
  • The Plant Journal, Vol. 94, Issue 3
  • DOI: 10.1111/tpj.13871

The role of COBRA ‐ LIKE 2 function, as part of the complex network of interacting pathways regulating Arabidopsis seed mucilage polysaccharide matrix organization
journal, March 2018

  • Ben‐Tov, Daniela; Idan‐Molakandov, Anat; Hugger, Anat
  • The Plant Journal, Vol. 94, Issue 3
  • DOI: 10.1111/tpj.13871

TRM 4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA 3
journal, September 2018

  • Yang, Bo; Voiniciuc, Cătălin; Fu, Lanbao
  • New Phytologist, Vol. 221, Issue 2
  • DOI: 10.1111/nph.15442