The Galactose Residues of Xyloglucan Are Essential to Maintain Mechanical Strength of the Primary Cell Walls in Arabidopsis during Growth1

In land plants, xyloglucans (XyGs) tether cellulose microfibrils into a strong but extensible cell wall. The MUR2 and MUR3 genes of Arabidopsis encode XyG-specific fucosyl and galactosyl transferases, respectively. Mutations of these genes give precisely altered XyG structures missing one or both of these subtending sugar residues. Tensile strength measurements of etiolated hypocotyls revealed that galactosylation rather than fucosylation of the side chains is essential for maintenance of wall strength. Symptomatic of this loss of tensile strength is an abnormal swelling of the cells at the base of fully grown hypocotyls as well as bulging and marked increase in the diameter of the epidermal and underlying cortical cells. The presence of subtending galactosyl residues markedly enhance the activities of XyG endotransglucosylases and the accessibility of XyG to their action, indicating a role for this enzyme activity in XyG cleavage and religation in the wall during growth for maintenance of tensile strength. Although a shortening of XyGs that normally accompanies cell elongation appears to be slightly reduced, galactosylation of the XyGs is not strictly required for cell elongation, for lengthening the polymers that occurs in the wall upon secretion, or for binding of the XyGs to cellulose.

[1]  K. Nishitani.  Construction and restructuring of the cellulose-xyloglucan framework in the apoplast as mediated by the xyloglucan-related protein family—A hypothetical scheme , 1998, Journal of Plant Research.

[2]  M. Gidley,et al.  A xyloglucan-oligosaccharide-specific α-d-xylosidase or exo-oligoxyloglucan-α-xylohydrolase from germinated nasturtium (Tropaeolum majus L.) seeds , 1991, Planta.

[3]  R. Cleland.  Extensibility of isolated cell walls: Measurement and changes during cell elongation , 1967, Planta.

[4]  S. McQueen-Mason,et al.  The relationship between xyloglucan endotransglycosylase and in-vitro cell wall extension in cucumber hypocotyls , 2004, Planta.

[5]  C. Dunand,et al.  The MUR3 Gene of Arabidopsis Encodes a Xyloglucan Galactosyltransferase That Is Evolutionarily Related to Animal Exostosins Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009837. , 2003, The Plant Cell Online.

[6]  Keiko Sugimoto-Shirasu,et al.  Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes1 , 2003, Plant Physiology.

[7]  K. Nishitani,et al.  The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. , 2002, Plant & cell physiology.

[8]  George Jeronimidis,et al.  Mechanical properties of primary plant cell wall analogues , 2002, Planta.

[9]  Takahisa Hayashi,et al.  Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  N. Raikhel,et al.  The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  K. Nishitani,et al.  A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. , 2001, Plant & cell physiology.

[12]  M. Pauly,et al.  Changes in the structure of xyloglucan during cell elongation , 2001, Planta.

[13]  J. Thompson,et al.  Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. , 2001, The Plant journal : for cell and molecular biology.

[14]  U. Sonnewald,et al.  Functional characterisation of Nicotiana tabacum xyloglucan endotransglycosylase (NtXET-1): generation of transgenic tobacco plants and changes in cell wall xyloglucan , 2001, Planta.

[15]  Daniel J. Cosgrove,et al.  Loosening of plant cell walls by expansins , 2000, Nature.

[16]  T. Nakamura,et al.  The isolation of wall‐bound proteins regulating yield threshold tension in glycerinated hollow cylinders of cowpea hypocotyl , 2000 .

[17]  A Darvill,et al.  Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. , 1999, The Plant journal : for cell and molecular biology.

[18]  M. Shirakawa,et al.  Gelation of Enzymatically Degraded Xyloglucan Extracted from Tamarind Seed (特集 繊維と結晶) , 1999 .

[19]  M. Buckeridge,et al.  Xyloglucan mobilisation and purification of a (XLLG/XLXG) specific β-galactosidase from cotyledons of Copaifera langsdorffii , 1999 .

[20]  P. Campbell,et al.  Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. , 1999, Trends in plant science.

[21]  S. Fry,et al.  Purification of xyloglucan endotransglycosylases (XETs): a generally applicable and simple method based on reversible formation of an enzyme-substrate complex. , 1999, The Biochemical journal.

[22]  J. Reid,et al.  A xyloglucan oligosaccharide-active, transglycosylating beta-D-glucosidase from the cotyledons of nasturtium (Tropaeolum majus L) seedlings--purification, properties and characterization of a cDNA clone. , 1998, The Plant journal : for cell and molecular biology.

[23]  K. Nishinari,et al.  Tailoring of xyloglucan properties using an enzyme , 1998 .

[24]  S. Fry,et al.  The Arabidopsis TCH4 Xyloglucan Endotransglycosylase (Substrate Specificity, pH Optimum, and Cold Tolerance) , 1997, Plant physiology.

[25]  C. Chapple,et al.  Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. , 1997, The Plant journal : for cell and molecular biology.

[26]  L. Staehelin,et al.  Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations. , 1997, The Plant journal : for cell and molecular biology.

[27]  C. Chapple,et al.  Substitution of l-Fucose by l-Galactose in Cell Walls of Arabidopsis mur1 , 1996, Science.

[28]  P. Albersheim,et al.  An unambiguous nomenclature for xyloglucan‐derived oligosaccharides , 1993 .

[29]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[30]  S. McQueen-Mason,et al.  Two endogenous proteins that induce cell wall extension in plants. , 1992, The Plant cell.

[31]  K. Nishitani,et al.  Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. , 1992, The Journal of biological chemistry.

[32]  S. Fry,et al.  Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. , 1992, The Biochemical journal.

[33]  L. D. Talbott,et al.  Changes in molecular size of previously deposited and newly synthesized pea cell wall matrix polysaccharides : effects of auxin and turgor. , 1992, Plant physiology.

[34]  B. Meyer,et al.  Simulations of the static and dynamic molecular conformations of xyloglucan. The role of the fucosylated sidechain in surface-specific sidechain folding. , 1991, The Plant journal : for cell and molecular biology.

[35]  J. Reid,et al.  A beta-D-galactosidase from nasturtium (Tropaeolum majus L.) cotyledons. Purification, properties, and demonstration that xyloglucan is the natural substrate. , 1988, The Journal of biological chemistry.

[36]  F. Smith,et al.  Colorimetric Method for Determination of Sugars and Related Substances , 1956 .