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 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.
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.) c.voiniciuc@fz-juelich.de.
authors.forename: Cătălin
authors.identifier: http://orcid.org/0000-0001-9105-014X
authors.initials: C
authors.lastname: Voiniciuc
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Maximilian Heinrich-Wilhelm
authors.identifier: http://orcid.org/0000-0003-4576-6774
authors.initials: MH
authors.lastname: Schmidt
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Adeline
authors.initials: A
authors.lastname: Berger
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Bo
authors.identifier: http://orcid.org/0000-0003-4446-0415
authors.initials: B
authors.lastname: Yang
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Berit
authors.initials: B
authors.lastname: Ebert
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Henrik V
authors.initials: HV
authors.lastname: Scheller
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Helen M
authors.initials: HM
authors.lastname: North
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Björn
authors.initials: B
authors.lastname: Usadel
authors.affiliation: Institute for Biosciences and Geosciences (Plant Sciences), Forschungszentrum Jülich, 52425 Juelich, Germany (C.V., M.H.-W.S., B.U., M.G.);Institute for Botany and Molecular Genetics, BioEconomy Science Center, RWTH Aachen University, 52056 Aachen, Germany (C.V., M.H.-W.S., B.Y., B.U.);Institut National de la Recherche Agronomique and AgroParisTech, Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318, ERL Centre National de la Recherche Scientifique 3559, Saclay Plant Sciences, F-78026 Versailles, France (A.B., H.M.N.);Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94702 (B.E., H.V.S.); andDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720 (H.V.S.).
authors.forename: Markus
authors.initials: M
authors.lastname: Günl
mesh_terms: D000268:Adhesiveness; D017360:Arabidopsis / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D020126:Brefeldin A / Q000494:pharmacology; D002118:Calcium / Q000378:metabolism; D002482:Cellulose / Q000378:metabolism*; D005964:Glucosyltransferases / Q000378:metabolism; D006031:Glycosylation / Q000187:drug effects; D006056:Golgi Apparatus / Q000378:metabolism; D008351:Mannans / Q000096:biosynthesis*; D009005:Monosaccharides / Q000032:analysis; D010368:Pectins / Q000378:metabolism*; D062087:Plant Mucilage / Q000378:metabolism*; D021381:Protein Transport; D012639:Seeds / Q000378:metabolism*; D017386:Sequence Homology, Amino Acid; D029910:Trigonella / Q000378:metabolism; D047071:beta-Glucans / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D008351:Mannans; D009005:Monosaccharides; D062087:Plant Mucilage; D047071:beta-Glucans; C443804:galactoglucomannan; D020126:Brefeldin A; D010368:Pectins; D002482:Cellulose; C000593207:CELLULOSE SYNTHASE-LIKE A2 protein, Arabidopsis; D005964:Glucosyltransferases; D002118:Calcium