Functional Diversity of Xyloglucan-Related Proteins and its Implications in the Cell Wall Dynamics in Plants

Abstract

The plant cell wall is a dynamic apparatus responsible for both morphogenesis and responsiveness to environmental conditions. In the cell wall of most seed plants, cellulose microfibrils are cross-linked by xyloglucans to form a cellulose/xyloglucan framework, which functions as the mechanical underpinning of the cell wall. Endoxyloglucan transferases are a class of enzymes that play a central role in construction and modification of the plant cell wall. These enzymes are encoded by a large multi-gene family termed xyloglucan-related proteins (XRPs). More than 24 members of the XRP family have so far been identified in Arabidopsis thaliana. Each member of this family functions as either a hydrolase or a transferase acting on xyloglucans. The primary structures of proteins and gene-expression profiles have strongly suggested their potentially divergent roles in plant morphogenesis: different members of this family are expressed in different types of tissues at distinct developmental stages and respond differentially to individual hormones as well as environmental stimuli. These facts imply that each member of this gene family is individually committed to a specific process that proceeds in a specific tissue at a specific stage of development. Probably the generation and maintenance of the cell walls in a whole organ, and thus in the whole plant, is achieved by the ensemble of individual members of the XRP family.

Abbreviations

EXGT: endoxyloglucan transferase

XET: xyloglucan endotransglycosylase

XRP: xyloglucan-related protein

Key words

Cell wall - cellulose - xyloglucan - endoxyloglucan transferase - genome - xyloglucan-related protein family

References

• 01 Akamatsu,  T.,, Hanzawa,  Y.,, Ohtake,  Y.,, Takahashi,  T.,, Nishitani,  K.,, and Komeda,  Y.. (1999);  Expression of endoxyloglucan transferase genes in acaulis mutants of Arabidopsis. .  Plant Physiol.. 121 715-721
• 02 Amor,  Y.,, Haigler,  C. H.,, Johnson,  S.,, Wainscott,  M.,, and Delmer,  D. P.. (1995);  A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants.  Proc. Natl. Acad. Sci. USA. 92 9353-9357
• 03 Arioli,  T.,, Peng,  L. C.,, Betzner,  A. S.,, Burn,  J.,, Wittke,  W.,, Herth,  W.,, Camilleri,  C.,, Hofte,  H.,, Plazinski,  J.,, Birch,  R.,, Cork,  A.,, Glover,  J.,, Redmond,  J.,, and Williamson,  R. E.. (1998);  Molecular analysis of cellulose biosynthesis in Arabidopsis. .  Science. 279 717-720
• 04 Aubert,  D., and Herzog,  M.. (1996);  A new cDNA encoding a xyloglucan endo-transglycosylase-related polypeptide (AtXTR8) preferentially expressed in seedling, root and stem of Arabidopsis thaliana.  Plant Sci.. 121 187-196
• 05 Barbeyron,  T.,, Gerard,  A.,, Potin,  P.,, Henrissat,  B.,, and Kloareg,  B.. (1998);  The kappa-carrageenase of the marine bacterium Cytophaga drobachiensis: structural and phylogenetic relationships within family-16 glycoside hydrolases.  Molecular Biology Evolution. 15 528-537
• 06 Brummell,  D. A.,, Camirand,  A.,, and Maclachlan,  G. A.. (1990);  Differential distribution of xyloglucan glycosyl transferases in pea Golgi dictyosomes and secretory vesicles.  J. Cell Sci.. 96 705-710
• 07 Campbell,  P., and Braam,  J.. (1998);  Co- and/or post-translational modifications are critical for TCH4 XET Activity.  Plant J.. 15 553-561
• 08 Campbell,  P., and Braam,  J.. (1999);  Xyloglucan endotransglycosylase: diversity of genes, enzymes and potential wall-modyfying functions.  Trends in Plant Sciences. 4 361-366
• 09 Campbell,  P., and Braam,  J.. (1999);  In vitro activities of four xyloglucan endotransglycosylases from Arabidopsis. .  Plant J.. 18 371-382
• 10 Carpita,  N. C., and Gibeaut,  D. M.. (1993);  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth.  Plant J.. 3 1-30
• 11 Catala,  C.,, Rose,  J. K. C.,, and Bennett,  A. B.. (1997);  Auxin regulation and spatial localization of an endo-1,4-β-D-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls.  Plant J.. 12 417-426
• 12 Cosgrove,  D. J.. (1997);  Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement.  Plant Cell. 9 1031-1041
• 13 Darvill,  A. G.,, McNeil,  M.,, Albersheim,  P.,, and Delmer,  D. P.. (1980) The primary cell walls of flowering plants. The Biochemistry of Plants, Vol. 1. Tolbert, N. E., ed. New York; Academic Press pp. 91-162
• 14 de Silva,  J.,, Jarman,  C. D.,, Arrowsmith,  D. A.,, Stronach,  M. S.,, Chengappa,  S.,, Sidebottom,  C.,, and Reid,  J. S.. (1993);  Molecular characterization of a xyloglucan-specific endo-(1→ 4)-β-D-glucanase (xyloglucan endo-transglycosylase) from nasturtium seeds.  Plant J.. 3 701-711
• 15 Fanutti,  C.,, Gidley,  M. J.,, and Reid,  J. S.. (1993);  Action of a pure xyloglucan endo-transglycosylase (formerly called xyloglucan-specific endo-(1→ 4)-β-D-glucanase) from the cotyledons of germinated nasturtium seeds.  Plant J.. 3 691-700
• 16 Fry,  S. C.,, Smith,  R. C.,, Renwick,  K. F.,, Martin,  D. J.,, Hodge,  S. K.,, and Matthews,  K. J.. (1992);  Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants.  Biochemical J.. 282 821-828
• 17 Henrissat,  B., and Bairoch,  A.. (1993);  New families in the classification of glycosyl hydrolases based on amino acid sequence similarities.  Biochemical J.. 293 781-788
• 18 Hoj,  P. B., and Fincher,  G. B.. (1995);  Molecular evolution of plant beta-glucan endohydrolases.  Plant J.. 7 367-379
• 19 Hyodo,  H.,, Takemura,  M.,, Yokota,  A.,, Ohyama,  K.,, and Kohchi,  T.. (2000);  Systematic isolation of highly transcribed genes in inflorescences apices in Arabidopsis thaliana from an equalized cDNA library.  Biosci. Biotechnol. Biochem.. 64 1538-1541
• 20 Ito,  H., and Nishitani,  K.. (1999);  Visualization of EXGT-mediated molecular grafting activity by means of a fluorescent-labeled xyloglucan oligomer.  Plant Cell Physiol.. 40 1172-1176
• 21 Juncosa,  M.,, Pons,  J.,, Dot,  T.,, Querol,  E.,, and Planas,  A.. (1994);  Identification of active site carboxylic residues in Bacillus licheniformis 1,3-1,4-β-D-glucan 4-glucanohydrolase by site-directed mutagenesis.  J. Biol. Chem.. 269 14530-14535
• 22 Keitel,  T.,, Simon,  O.,, Borriss,  R.,, and Heinemann,  U.. (1993);  Molecular and active-site structure of a Bacillus 1,3-1,4-β-glucanase.  Proc. Natl. Acad. Sci. USA. 90 5287-5291
• 23 Kutschera,  U.. (1994);  The current status of the acid-growth hypothesis.  New Phytol.. 126 549-569
• 24 Lashbrook,  C. C.,, Gonzalez-Bosch,  C.,, and Bennett,  A. B.. (1994);  Two divergent endo-β-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers.  Plant Cell. 6 1485-1493
• 25 Lerouge,  P.,, Fitchette-Lain,  A.-C.,, Chekkafi,  A.,, Avidgor,  V.,, and Faye,  L.. (1996);  N-linked oligosaccharide processing is not necessary for glycoprotein secretion in plants.  Plant J.. 10 713-719
• 26 McQueen-Mason,  S.,, Durachko,  D. M.,, and Cosgrove,  D. J.. (1992);  Two endogenous proteins that induce cell wall extension in plants.  Plant Cell. 4 1425-1433
• 27 Medford,  J. I.,, Elmer,  J. S.,, and Klee,  H. J.. (1991);  Molecular cloning and characterization of genes expressed in shoot apical meristems.  Plant Cell. 3 359-370
• 28 Nishitani,  K.. (1995);  Endo-xyloglucan transferase, a new class of transferase involved in cell wall construction.  J. Plant Res.. 108 137-148
• 29 Nishitani,  K.. (1997);  The role of endoxyloglucan transferase in the organization of plant cell walls.  Int. Rev. Cytol.. 173 157-206
• 30 Nishitani,  K.. (1998);  Construction and restructuring of the cellulose-xyloglucan framework in the apoplast as mediated by the xyloglucan-related protein family: a hypothetical scheme.  J. Plant Res.. 111 159-166
• 31 Nishitani,  K., and Tominaga,  R.. (1991);  In vitro molecular weight increase in xyloglucans by an apoplastic enzyme preparation from epicotyls of Vigna angularis. .  Physiol. Plant. 82 490-497
• 32 Nishitani,  K., and Tominaga,  R.. (1992);  Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule.  J. Biol. Chem.. 267 21058-21064
• 33 Okamoto-Nakazato,  A.,, Nakamura,  T.,, and Okamoto,  H.. (2000);  The isolation of wall-bound proteins regulating yield threshold tension in glycerinated hollow cylinders of cowpea hypocotyl.  Plant Cell Environment. 23 145-154
• 34 Okamoto-Nakazato,  A.,, Takahashi,  K.,, Kido,  N.,, Owaribe,  K.,, and Katou,  K.. (2000);  Molecular cloning of yieldins regulating the yield threshold of cowpea cell walls: cDNA cloning and characterization of recombinant yieldin.  Plant Cell Environment. 23 155-164
• 35 Okazawa,  K.,, Sato,  Y.,, Nakagawa,  T.,, Asada,  K.,, Kato,  I.,, Tomita,  E.,, and Nishitani,  K.. (1993);  Molecular cloning and cDNA sequencing of endoxyloglucan transferase, a novel class of glycosyltransferase that mediates molecular grafting between matrix polysaccharides in plant walls.  J. Biol. Chem.. 268 25364-25368
• 36 Pear,  J. R.,, Kawagoe,  Y.,, Schreckengost,  W. E.,, Delmer,  D. P.,, and Stalker,  D. M.. (1996);  Higher plants contain homologs of the bacterial ce/A genes encoding the catalytic subunit of cellulose synthase.  Proc. Natl. Acad. Sci. USA. 93 12637-12642
• 37 Rose,  J. K. C.,, Brummell,  D. A.,, and Bennett,  A. B.. (1996);  Two divergent xyloglucan endotransglycosylases exhibit mutually exclusive patterns of expression in nasturtium.  Plant Physiol.. 110 493-499
• 38 Sachs,  J. V.. (1887) Lectures on the physiology of plants (translated by H. M. Ward). Oxford; The Clarendon Press
• 39 Sakurai,  N.. (1998);  Dynamic function and regulation of apoplast in the plant body.  J. of Plant Res.. 111 133-148
• 40 Tabuchi,  A.,, Kamisaka,  S.,, and Hoson,  T.. (1997);  Purification of xyloglucan hydrolase/endotransferase from cell walls of azuki bean epicotyls.  Plant Cell Physiol.. 38 653-658
• 41 Takano,  M.,, Fujii,  N.,, Higashitani,  A.,, Nishitani,  K.,, Hirasawa,  T.,, and Takahashi,  H.. (1999);  Endoxyloglucan transferase cDNA isolated from pea roots and its fluctuating expression in hydrotropically responding roots.  Plant Cell Physiol.. 40 135-142
• 42 Tucker,  M. L., and Milligan,  S. B.. (1991);  Sequence analysis and comparison of avocado fruit and bean abscission cellulases.  Plant Physiol.. 95 928-933
• 43 Xu,  W.,, Campbell,  P.,, Vargheese,  A. V.,, and Braam,  J.. (1996);  The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression.  Plant J.. 9 879-889
• 44 Xu,  W.,, Purugganan,  M.,, Polisensky,  D. H.,, Antosiewicz,  D. M.,, Fry,  S. C.,, and Braam,  J.. (1995);  Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase.  Plant Cell. 7 1555-1567
• 45 Zablackis,  E.,, Huang,  J.,, Muller,  B.,, Darvill,  A. G.,, and Albersheim,  P.. (1995);  Structure of plant cell walls. 39. Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves.  Plant Physiol.. 107 1129-1138
• 46 Zhang,  G. F., and Staehelin,  L. A.. (1992);  Functional compartmentation of the Golgi apparatus of plant cells.  Plant Physiol.. 99 1070-1083

Section Editor: T. Nagata