title: Galactose-depleted xyloglucan is dysfunctional and leads to dwarfism in Arabidopsis.
abstract: Xyloglucan is a polysaccharide that has important roles in the formation and function of the walls that surround growing land plant cells. Many of these plants synthesize xyloglucan that contains galactose in two different side chains (L and F), which exist in distinct molecular environments. However, little is known about the contribution of these side chains to xyloglucan function. Here, we show that Arabidopsis (Arabidopsis thaliana) mutants devoid of the F side chain galactosyltransferase MURUS3 (MUR3) form xyloglucan that lacks F side chains and contains much less galactosylated xylose than its wild-type counterpart. The galactose-depleted xyloglucan is dysfunctional, as it leads to mutants that are dwarfed with curled rosette leaves, short petioles, and short inflorescence stems. Moreover, cell wall matrix polysaccharides, including xyloglucan and pectin, are not properly secreted and instead accumulate within intracellular aggregates. Near-normal growth is restored by generating mur3 mutants that produce no detectable amounts of xyloglucan. Thus, cellular processes are affected more by the presence of the dysfunctional xyloglucan than by eliminating xyloglucan altogether. To identify structural features responsible for xyloglucan dysfunction, xyloglucan structure was modified in situ by generating mur3 mutants that lack specific xyloglucan xylosyltransferases (XXTs) or that overexpress the XYLOGLUCAN L-SIDE CHAIN GALACTOSYLTRANSFERASE2 (XLT2) gene. Normal growth was restored in the mur3-3 mutant overexpressing XLT2 and in mur3-3 xxt double mutants when the dysfunctional xyloglucan was modified by doubling the amounts of galactosylated side chains. Our study assigns a role for galactosylation in normal xyloglucan function and demonstrates that altering xyloglucan side chain structure disturbs diverse cellular and physiological processes.
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Yingzhen
authors: Y
authors: Kong
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Maria J
authors: MJ
authors: Peña
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Luciana
authors: L
authors: Renna
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Utku
authors: U
authors: Avci
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Sivakumar
authors: S
authors: Pattathil
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Sami T
authors: ST
authors: Tuomivaara
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Xuemei
authors: X
authors: Li
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Wolf-Dieter
authors: WD
authors: Reiter
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Federica
authors: F
authors: Brandizzi
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Michael G
authors: MG
authors: Hahn
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: Alan G
authors: AG
authors: Darvill
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.).
authors: William S
authors: WS
authors: York
authors: Complex Carbohydrate Research Center (Y.K., M.J.P., U.A., S.P., S.T.T., M.G.H., A.G.D., W.S.Y., M.A.O.), Department of Plant Biology (M.G.H.), and Department of Biochemistry and Molecular Biology (A.G.D., W.S.Y.), University of Georgia, Athens, Georgia 30602;Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, Shandong 266101, China (Y.K.);United States Department of Energy Plant Research Laboratory (L.R., F.B.) and United States Department of Energy Great Lakes Bioenergy Research Center (F.B.), Michigan State University, East Lansing, Michigan 48824; andDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269 (X.L., W.-D.R.) mao@ccrc.uga.edu.
authors: Malcolm A
authors: MA
authors: O'Neill
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002473:Cell Wall / Q000737:chemistry; D005690:Galactose / Q000378:metabolism*; D005700:Galactosyltransferases / Q000235:genetics / Q000378:metabolism*; D005936:Glucans / Q000737:chemistry / Q000378:metabolism*; D056626:Inflorescence / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D009154:Mutation; D010368:Pectins / Q000378:metabolism; D010641:Phenotype; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D018547:Plant Stems / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D011134:Polysaccharides / Q000378:metabolism; D014990:Xylans / Q000737:chemistry / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D005936:Glucans; D011134:Polysaccharides; D014990:Xylans; C029353:xyloglucan; D010368:Pectins; D005700:Galactosyltransferases; C478982:MUR3 protein, Arabidopsis; C000604702:XLT2 protein, Arabidopsis; C047006:N-acetyllactosaminide alpha-1,3-galactosyltransferase; D005690:Galactose