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

Journal Article · · Plant Physiology (Bethesda)
DOI:https://doi.org/10.1104/pp.15.00851· OSTI ID:1512244
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

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Natural Sciences and Engineering Research Council of Canada (NSERC)
Grant/Contract Number:
AC02-05CH11231; 313/323–400–00213
OSTI ID:
1512244
Journal Information:
Plant Physiology (Bethesda), Vol. 169, Issue 1; ISSN 0032-0889
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 90 works
Citation information provided by
Web of Science

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Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis journal June 2016
Evolution of protein N-glycosylation process in Golgi apparatus which shapes diversity of protein N-glycan structures in plants, animals and fungi journal January 2017
Mechanistic insights from plant heteromannan synthesis in yeast journal December 2018
Plant genome and transcriptome annotations: from misconceptions to simple solutions journal January 2017
TRM 4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA 3 journal September 2018
Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants journal June 2019
Regulatory-associated protein of TOR (RAPTOR) alters the hormonal and metabolic composition of Arabidopsis seeds, controlling seed morphology, viability and germination potential journal September 2017
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
Functional conservation and divergence of Miscanthus lutarioriparius GT43 gene family in xylan biosynthesis journal April 2016
MuSeeQ, a novel supervised image analysis tool for the simultaneous phenotyping of the soluble mucilage and seed morphometric parameters journal December 2018
A small-scale fractionation pipeline for rapid analysis of seed mucilage characteristics journal February 2020
Removal of glucuronic acid from xylan is a strategy to improve the conversion of plant biomass to sugars for bioenergy journal September 2017
The micro- and nanoscale spatial architecture of the seed mucilage—Comparative study of selected plant species journal July 2018
Valorization of Sida (Sida hermaphrodita) biomass for multiple energy purposes text January 2017
Extensive Natural Variation in Arabidopsis Seed Mucilage Structure journal June 2016
Identification, Characterization, and Expression Analysis of Cell Wall Related Genes in Sorghum bicolor (L.) Moench, a Food, Fodder, and Biofuel Crop journal August 2016
Cytochemical Localization of Polysaccharides in Dendrobium officinale and the Involvement of DoCSLA6 in the Synthesis of Mannan Polysaccharides journal February 2017
Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression journal July 2019
Emerging Functions for Cell Wall Polysaccharides Accumulated during Eudicot Seed Development journal September 2018
The Suitability of Orthogonal Hosts to Study Plant Cell Wall Biosynthesis journal November 2019
Valorization of Sida ( Sida hermaphrodita ) biomass for multiple energy purposes journal May 2016
Extensive Natural Variation in Arabidopsis Seed Mucilage Structure text January 2016
Plant genome and transcriptome annotations : from misconceptions to simple solutions text January 2018
Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis text January 2016
Removal of glucuronic acid from xylan is a strategy to improve the conversion of plant biomass to sugars for bioenergy text January 2017
TRM4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA3 text January 2019
Removal of glucuronic acid from xylan is a strategy to improve the conversion of plant biomass to sugars for bioenergy text January 2017
Xylan synthesized by Irregular Xylem 14 ( IRX14 ) maintains the structure of seed coat mucilage in Arabidopsis journal February 2016
PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification journal February 2016
Differences in glycosyltransferase family 61 accompany variation in seed coat mucilage composition in Plantago spp. journal November 2016
Heterologous expression and characterization of an Arabidopsis β-l-arabinopyranosidase and α-d-galactosidases acting on β-l-arabinopyranosyl residues journal July 2017
T-6b allocates more assimilation product for oil synthesis and less for polysaccharide synthesis during the seed development of Arabidopsis thaliana journal January 2017
Overexpression of Grain Amaranth (Amaranthus hypochondriacus) AhERF or AhDOF Transcription Factors in Arabidopsis thaliana Increases Water Deficit- and Salt-Stress Tolerance, Respectively, via Contrasting Stress-Amelioration Mechanisms journal October 2016
Dissecting Seed Mucilage Adherence Mediated by FEI2 and SOS5 journal July 2016
Insight on Extraction and Characterisation of Biopolymers as the Green Coagulants for Microalgae Harvesting journal May 2020

Figures / Tables (14)


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