The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature.

The polysaccharide xyloglucan is thought to play an important structural role in the primary cell wall of dicotyledons. Accordingly, there is considerable interest in understanding the biochemical basis and regulation of xyloglucan metabolism, and research over the last 16 years has identified a large family of cell wall proteins that specifically catalyze xyloglucan endohydrolysis and/or endotransglucosylation. However, a confusing and contradictory series of nomenclatures has emerged in the literature, of which xyloglucan endotransglycosylases (XETs) and endoxyloglucan transferases (EXGTs) are just two examples, to describe members of essentially the same class of genes/proteins. The completion of the first plant genome sequencing projects has revealed the full extent of this gene family and so this is an opportune time to resolve the many discrepancies in the database that include different names being assigned to the same gene. Following consultation with members of the scientific community involved in plant cell wall research, we propose a new unifying nomenclature that conveys an accurate description of the spectrum of biochemical activities that cumulative research has shown are catalyzed by these enzymes. Thus, a member of this class of genes/proteins will be referred to as a xyloglucan endotransglucosylase/hydrolase (XTH). The two known activities of XTH proteins are referred to enzymologically as xyloglucan endotransglucosylase (XET, which is hereby re-defined) activity and xyloglucan endohydrolase (XEH) activity. This review provides a summary of the biochemical and functional diversity of XTHs, including an overview of the structure and organization of the Arabidopsis XTH gene family, and highlights the potentially important roles that XTHs appear to play in numerous examples of plant growth and development.

[1]  K. Nishitani Digital Object Identifier (DOI) 10.1007/s10265-002-0032-z JPR SYMPOSIUM , 2022 .

[2]  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.

[3]  K. Nishitani,et al.  The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf‐cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell‐wall formation , 2002, The EMBO journal.

[4]  K. Bradford,et al.  A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. , 2002, Journal of experimental botany.

[5]  A. Tabuchi,et al.  Action of xyloglucan hydrolase within the native cell wall architecture and its effect on cell wall extensibility in azuki bean epicotyls. , 2002, Plant & cell physiology.

[6]  Hongyu Zhao,et al.  Light Control of Arabidopsis Development Entails Coordinated Regulation of Genome Expression and Cellular Pathways , 2001, The Plant Cell Online.

[7]  R. Baran,et al.  Release of complexed xyloglucan endotransglycosylase (XET) from plant cell walls by a transglycosylation reaction with xyloglucan-derived oligosaccharides , 2001 .

[8]  J. Verbelen,et al.  Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. , 2001, Plant physiology.

[9]  A. Bennett,et al.  Characterization of a tomato xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls. , 2001, Plant physiology.

[10]  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.

[11]  Z. Sulová,et al.  Ten isoenzymes of xyloglucan endotransglycosylase from plant cell walls select and cleave the donor substrate stochastically. , 2001, The Biochemical journal.

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

[13]  K. Nishitani,et al.  Endoxyloglucan transferase is localized both in the cell plate and in the secretory pathway destined for the apoplast in tobacco cells. , 2001, Plant & cell physiology.

[14]  H. Mori,et al.  A new type of endo-xyloglucan transferase devoted to xyloglucan hydrolysis in the cell wall of azuki bean epicotyls. , 2001, Plant & cell physiology.

[15]  Stephen C. Fry,et al.  The Growing Plant Cell Wall: Chemical and Metabolic Analysis , 2001 .

[16]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[17]  R. Baran,et al.  Ping-pong character of nasturtium-seed xyloglucan endotransglycosylase (XET) reaction. , 2000, General physiology and biophysics.

[18]  K. Nishitani,et al.  Functional Diversity of Xyloglucan-Related Proteins and its Implications in the Cell Wall Dynamics in Plants , 2000 .

[19]  S. Fry,et al.  Differences in catalytic properties between native isoenzymes of xyloglucan endotransglycosylase (XET). , 2000, Phytochemistry.

[20]  J. Verbelen,et al.  In Vivo Colocalization of Xyloglucan Endotransglycosylase Activity and Its Donor Substrate in the Elongation Zone of Arabidopsis Roots , 2000, Plant Cell.

[21]  M. Delseny,et al.  Extensive Duplication and Reshuffling in the Arabidopsis Genome , 2000, Plant Cell.

[22]  J. Burstin Differential expression of two barley XET-related genes during coleoptile growth. , 2000, Journal of experimental botany.

[23]  M. Matsuoka,et al.  Characterization of XET-related genes of rice. , 2000, Plant physiology.

[24]  A. Bennett,et al.  Auxin-regulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth. , 2000, Plant physiology.

[25]  K. Nishitani,et al.  Expression of endoxyloglucan transferase genes in acaulis mutants of Arabidopsis. , 1999, Plant physiology.

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

[27]  P. Iannetta,et al.  Visualization of the activity of xyloglucan endotransglycosylase (XET) isoenzymes after gel electrophoresis , 1999 .

[28]  P. Campbell,et al.  In vitro activities of four xyloglucan endotransglycosylases from Arabidopsis. , 1999, The Plant journal : for cell and molecular biology.

[29]  A. Bennett,et al.  Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. , 1999, Trends in plant science.

[30]  I. Maldonado-Mendoza,et al.  Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. , 1999, Molecular plant-microbe interactions : MPMI.

[31]  P. Campbell,et al.  Co- and/or post-translational modifications are critical for TCH4 XET activity. , 1998, The Plant journal : for cell and molecular biology.

[32]  Z. Sulová,et al.  Xyloglucan endotransglycosylase: evidence for the existence of a relatively stable glycosyl-enzyme intermediate. , 1998, The Biochemical journal.

[33]  R. Atkinson,et al.  Biochemical and molecular characterisation of xyloglucan endotransglycosylase from ripe kiwifruit , 1998, Planta.

[34]  J. Braam,et al.  Cellular Localization of Arabidopsis Xyloglucan Endotransglycosylase-Related Proteins during Development and after Wind Stimulation , 1997, Plant physiology.

[35]  P. H. Schünmann,et al.  Expression of XET‐related genes and its relation to elongation in leaves of barley (Hordeum vulgare L.) , 1997 .

[36]  J. Thompson,et al.  Xyloglucan undergoes interpolymeric transglycosylation during binding to the plant cell wall in vivo: evidence from 13C/3H dual labelling and isopycnic centrifugation in caesium trifluoroacetate. , 1997, The Biochemical journal.

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

[38]  A. Bennett,et al.  Auxin regulation and spatial localization of an endo-1,4-beta-D-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls. , 1997, The Plant journal : for cell and molecular biology.

[39]  J. Medford,et al.  Modified MERI5 expression alters cell expansion in transgenic Arabidopsis plants , 1997 .

[40]  T. Matsumoto,et al.  A Xyloglucan-Specific Endo-1,4-[beta]-Glucanase Isolated from Auxin-Treated Pea Stems , 1997, Plant physiology.

[41]  S. Fry Novel 'dot-blot' assays for glycosyltransferases and glycosylhydrolases: Optimization for xyloglucan endotransglycosylase (XET) activity , 1997 .

[42]  E. P. Lorences,et al.  Effect of Xyloglucan Oligosaccharides on Growth, Viscoelastic Properties, and Long-Term Extension of Pea Shoots , 1997, Plant physiology.

[43]  T. Takeda,et al.  Xyloglucan endotransglycosylation in suspension-cultured poplar cells. , 1996, Bioscience, biotechnology, and biochemistry.

[44]  D. Aubert,et al.  A new cDNA encoding a xyloglucan endo-transglycosylase-related polypeptide (AtXTR8) preferentially expressed in seedling, root and stem of Arabidopsis thaliana , 1996 .

[45]  M. Gidley,et al.  Substrate subsite recognition of the xyloglucan endo-transglycosylase or xyloglucan-specific endo-(1→4)-β-d-glucanase from the cotyledons of germinated nasturtium (Tropaeolum majus L.) seeds , 1996, Planta.

[46]  P. Chandler,et al.  The regulation of leaf elongation and xyloglucan endotransglycosylase by gibberellin in ‘Himalaya’ barley (Hordeum vulgare L.) , 1996 .

[47]  M. Sachs,et al.  A Flooding-Induced Xyloglucan Endo-Transglycosylase Homolog in Maize Is Responsive to Ethylene and Associated with Aerenchyma , 1996, Plant physiology.

[48]  P. Campbell,et al.  The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression. , 1996, The Plant journal : for cell and molecular biology.

[49]  W. Davies,et al.  An analysis of relative elemental growth rate, epidermal cell size and xyloglucan endotransglycosylase activity through the growing zone of ageing maize leaves , 1996 .

[50]  A. Bennett,et al.  Two Divergent Xyloglucan Endotransglycosylases Exhibit Mutually Exclusive Patterns of Expression in Nasturtium , 1996, Plant physiology.

[51]  S. Fry,et al.  Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. , 1995, The Plant cell.

[52]  Z. Sulová,et al.  A colorimetric assay for xyloglucan-endotransglycosylase from germinating seeds. , 1995, Analytical biochemistry.

[53]  J. D. Silva,et al.  Characterisation of two tomato fruit-expressed cDNAs encoding xyloglucan endo-transglycosylase , 1995, Plant Molecular Biology.

[54]  S. Fry,et al.  Changes in xyloglucan endotransglycosylase (XET) activity during hormone-induced growth in lettuce and cucumber hypocotyls and spinach veil suspension cultures , 1994 .

[55]  S. Robinson,et al.  Xyloglucan endotransglycosylase and plant growth , 1994 .

[56]  B. Pickard,et al.  Differential Changes in Size Distribution of Xyloglucan in the Cell Walls of Gravitropically Responding Pisum sativum Epicotyls , 1994, Plant physiology.

[57]  C. Brady,et al.  Endo-1,4-[beta]-Glucanase, Xyloglucanase, and Xyloglucan Endo-Transglycosylase Activities Versus Potential Substrates in Ripening Tomatoes , 1994, Plant physiology.

[58]  S. Fry,et al.  Implication of persimmon fruit hemicellulose metabolism in the softening process. Importance of xyloglucan endotransglycosylase , 1994 .

[59]  M. Sachs,et al.  Characterization and Expression of Transcripts Induced by Oxygen Deprivation in Maize (Zea mays L.) , 1994, Plant physiology.

[60]  S. Clouse,et al.  Molecular Cloning and Characterization of a Brassinosteroid-Regulated Gene from Elongating Soybean (Glycine max L.) Epicotyls , 1994, Plant physiology.

[61]  S. Fry,et al.  Xyloglucan Endotransglycosylase Activity Increases during Kiwifruit (Actinidia deliciosa) Ripening (Implications for Fruit Softening) , 1993, Plant physiology.

[62]  S. Fry,et al.  Xyloglucan Endotransglycosylase Activity in Carrot Cell Suspensions during cell Elongation and Somatic Embryogenesis , 1993, Plant physiology.

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

[64]  S. Fry,et al.  Xyloglucan Endotransglycosylase Activity in Pea Internodes [Effects of Applied Gibberellic Acid] , 1993, Plant physiology.

[65]  Jeremy Pritchard,et al.  Xyloglucan Endotransglycosylase Activity, Microfibril Orientation and the Profiles of Cell Wall Properties Along Growing Regions of Maize Roots , 1993 .

[66]  S. Fry,et al.  Xyloglucan oligosaccharides with at least two α-d-xylose residues act as acceptor substrates for xyloglucan endotransglycosylase and promote the depolymerisation of xyloglucan , 1993 .

[67]  Z. Sulová,et al.  Cleavage of xyloglucan by nasturtium seed xyloglucanase and transglycosylation to xyloglucan subunit oligosaccharides. , 1992, Archives of biochemistry and biophysics.

[68]  Maureen C. McCann,et al.  Complexity in the spatial localization and length distribution of plant cell‐wall matrix polysaccharides , 1992 .

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

[70]  S. Fry,et al.  Endotransglycosylation of xyloglucans in plant cell suspension cultures. , 1991, The Biochemical journal.

[71]  K. Nishitani,et al.  In vitro molecular weight increase in xyloglucans by an apoplastic enzyme preparation from epicotyls of Vigna angularis , 1991 .

[72]  J. Medford,et al.  Molecular cloning and characterization of genes expressed in shoot apical meristems. , 1991, The Plant cell.

[73]  G. McDougall,et al.  Xyloglucan oligosaccharides promote growth and activate cellulase: evidence for a role of cellulase in cell expansion. , 1990, Plant physiology.

[74]  Ronald W. Davis,et al.  Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis , 1990, Cell.

[75]  S. Fry,et al.  In vivo Degradation and Extracellular Polymer-Binding of Xyloglucan Nonasaccharide, a Naturally-Occurring Anti-Auxin , 1989 .

[76]  S. Fry Cellulases, hemicelluloses and auxin‐stimulated growth: a possible relationship , 1989 .

[77]  S. Fry In-vivo formation of xyloglucan nonasaccharide: A possible biologically active cell-wall fragment , 1986, Planta.

[78]  N. L. Biddington,et al.  The effects of mechanically-induced stress in plants — a review , 1986, Plant Growth Regulation.

[79]  K. Nishitani,et al.  Acid pH-Induced Structural Changes in Cell Wall Xyloglucans in Vigna Angularis Epicotyl Segments , 1982 .

[80]  J. Labavitch,et al.  Turnover of cell wall polysaccharides in elongating pea stem segments. , 1974, Plant physiology.

[81]  R. Robinson Phytochemistry , 1962, Nature.

[82]  C. J. Chamberlain The Cell Wall , 1907, Botanical Gazette.

[83]  P. Schopfer,et al.  Inhibition of Golgi-apparatus function by brefeldin A in maize coleoptiles and its consequences on auxin-mediated growth, cell-wall extensibility and secretion of cell-wall proteins , 2004, Planta.

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

[85]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[86]  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.

[87]  Y. Nakamura,et al.  A large scale analysis of cDNA in Arabidopsis thaliana: generation of 12,028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. , 2000, DNA research : an international journal for rapid publication of reports on genes and genomes.

[88]  Nicholas C. Carpita,et al.  The cell wall , 2000 .

[89]  K. Nishitani,et al.  Visualization of EXGT-Mediated Molecular Grafting Activity by Means of a Fluorescent-Labeled Xyloglucan Oligomer , 1999 .

[90]  S. Clouse,et al.  Soybean BRU1 Encodes a Functional Xyloglucan Endotransglycosylase That is Highly Expressed in Inner Epicotyl Tissues during Brassinosteroid-Promoted Elongation , 1998 .

[91]  K. Nishitani The role of endoxyloglucan transferase in the organization of plant cell walls. , 1997, International review of cytology.

[92]  A. Tabuchi,et al.  Purification of Xyloglucan Hydrolase/Endotransferase from Cell Walls of Azuki Bean Epicotyls , 1997 .

[93]  M. Gidley,et al.  Action of a pure xyloglucan endo-transglycosylase (formerly called xyloglucan-specific endo-(1-->4)-beta-D-glucanase) from the cotyledons of germinated nasturtium seeds. , 1993, The Plant journal : for cell and molecular biology.

[94]  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.

[95]  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.

[96]  G. McDougall,et al.  Oligosaccharins from xyloglucan and cellulose: modulators of the action of auxin and H+ on plant growth. , 1990, Symposia of the Society for Experimental Biology.

[97]  M. Venis,et al.  Hormone perception and signal transduction in animals and plants. , 1990 .

[98]  Takahisa Hayashi,et al.  Xyloglucans in the Primary Cell Wall , 1989 .

[99]  P. Albersheim 9 – The Primary Cell Wall , 1976 .

[100]  K. Laidler The chemical kinetics of enzyme action , 1973 .

[101]  D. Lamport The primary cell wall , 1964 .