How do cell walls regulate plant growth?

The cell wall of growing plant tissues has frequently been interpreted in terms of inextensible cellulose microfibrils 'tethered' by hemicellulose polymers attached to the microfibril surface by hydrogen bonds, with growth occurring when tethers are broken or 'peeled' off the microfibril surface by expansins. This has sometimes been described as the 'sticky network' model. In this paper, a number of theoretical difficulties with this model, and discrepancies between predicted behaviour and observations by a number of researchers, are noted. (i) Predictions of cell wall moduli, based upon the sticky network model, suggest that the cell wall should be much weaker than is observed. (ii) The maximum hydrogen bond energy between tethers and microfibrils is less than the work done in expansion and therefore breakage of such hydrogen bonds is unlikely to limit growth. (iii) Composites of bacterial cellulose with xyloglucan are weaker than pellicles of pure cellulose so that it seems unlikely that hemicelluloses bind the microfibrils together. (iv) Calcium chelators promote creep of plant material in a similar way to expansins. (v) Reduced relative 'permittivities' inhibit the contraction of cell wall material when an applied stress is decreased. Revisions of the sticky network model that might address these issues are considered, as are alternatives including a model of cell wall biophysics in which cell wall polymers act as 'scaffolds' to regulate the space available for microfibril movement. Experiments that support the latter hypothesis, by demonstrating that reducing cell wall free volume decreases extensibility, are briefly described.

[1]  K. Waldron,et al.  Physiology and Biochemistry of Plant Cell Walls , 1990, Topics in Plant Physiology.

[2]  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.

[3]  T. Hoson.  Effect of Auxin on Autolysis of Cell Walls in Azuki Bean Epicotyls , 1990 .

[4]  D J Cosgrove,et al.  Expansive growth of plant cell walls. , 2000, Plant physiology and biochemistry : PPB.

[5]  S. McQueen-Mason,et al.  The molecular basis of plant cell wall extension , 2004, Plant Molecular Biology.

[6]  D. Burritt,et al.  Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils , 2000, Planta.

[7]  J. Sugiyama,et al.  Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. , 2003, The Plant journal : for cell and molecular biology.

[8]  D J Cosgrove,et al.  Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Cosgrove.  Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls. , 1989, Planta.

[10]  G. Jeronimidis,et al.  Mechanical effects of plant cell wall enzymes on cellulose/xyloglucan composites. , 2004, The Plant journal : for cell and molecular biology.

[11]  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 .

[12]  A. Mouradov,et al.  Two pine endo-beta-1,4-glucanases are associated with rapidly growing reproductive structures. , 1998, Plant physiology.

[13]  K. Owaribe,et al.  Molecular cloning of yieldins regulating the yield threshold of cowpea cell walls: cDNA cloning and characterization of recombinant yieldin. , 2000 .

[14]  M. L. Miller,et al.  The structure of polymers , 1966 .

[15]  M. Gidley,et al.  Probing expansin action using cellulose/hemicellulose composites. , 2000, The Plant journal : for cell and molecular biology.

[16]  D. S. Thompson.  Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit. , 2001, Journal of experimental botany.

[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]  P. Schopfer,et al.  Viscoelastic versus plastic cell wall extensibility in growing seedling organs: a contribution to avoid some misconceptions , 1997 .

[19]  Gidley,et al.  In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites , 1999, The Plant Journal.

[20]  Maureen C. McCann,et al.  Direct visualization of cross-links in the primary plant cell wall , 1990 .

[21]  D. Cosgrove.  Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. , 1997, The Plant cell.

[22]  Leslie H. Sperling,et al.  Polymeric Multicomponent Materials: An Introduction , 1997 .

[23]  R. Sexton.  Some ultrastructural observations on the nature of foliar abscission in Impatiens sultani , 2004, Planta.

[24]  J. Lockhart.  An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[25]  D. Delmer,et al.  Determination of the Pore Size of Cell Walls of Living Plant Cells , 1979, Science.

[26]  Sheh-Yi Sheu,et al.  Energetics of hydrogen bonds in peptides , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Cosgrove,et al.  Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Schopfer,et al.  Metabolic involvement in acid-mediated extension growth of maize coleoptiles , 1997 .

[29]  R Y Tsien,et al.  New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. , 1980, Biochemistry.

[30]  C. Quirós.  Celery: Apium graveolens L. , 1993 .

[31]  G. Wasteneys,et al.  Mutation or Drug-Dependent Microtubule Disruption Causes Radial Swelling without Altering Parallel Cellulose Microfibril Deposition in Arabidopsis Root Cells Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/t , 2003, The Plant Cell Online.

[32]  Stephen C. Fry,et al.  Turgor and Cell Expansion: Beyond the Lockhart Equation , 1992 .

[33]  S. Matsuoka,et al.  Relaxation Phenomena in Polymers , 1992 .

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

[35]  S. McQueen-Mason,et al.  Expansin Mode of Action on Cell Walls (Analysis of Wall Hydrolysis, Stress Relaxation, and Binding) , 1995, Plant physiology.

[36]  Models of Xyloglucan Binding to Cellulose Microfibrils1 , 1995 .

[37]  J. Passioura.  The physical chemistry of the primary cell wall: implications for the control of expansion rate , 1994 .

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

[39]  A. Peterlin,et al.  Molecular model of drawing polyethylene and polypropylene , 1971 .

[40]  L. D. Talbott,et al.  Molecular size and separability features of pea cell wall polysaccharides : implications for models of primary wall structure. , 1992, Plant physiology.

[41]  D J Cosgrove,et al.  A model of cell wall expansion based on thermodynamics of polymer networks. , 1998, Biophysical journal.

[42]  Elspeth MacRae,et al.  In vivo and in vitro swelling of cell walls during fruit ripening , 1997, Planta.

[43]  M. Canny.  Tansley Review No. 22 What becomes of the transpiration stream? , 1990, The New phytologist.

[44]  D. Burritt,et al.  Celery (Apium graveolens) parenchyma cell walls: cell walls with minimal xyloglucan. , 2002, Physiologia plantarum.

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

[46]  M. Tepfer,et al.  Long-term acid-induced wall extension in an in-vitro system , 2004, Planta.

[47]  P. Schopfer,et al.  Physical extensibility of maize coleoptile cell walls: apparent plastic extensibility is due to elastic hysteresis , 1992, Planta.

[48]  P. Schopfer,et al.  Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. , 2002, The Plant journal : for cell and molecular biology.

[49]  Mitchell,et al.  Roles of cellulose and xyloglucan in determining the mechanical properties of primary plant cell walls , 1999, Plant physiology.

[50]  Warren P. Mason,et al.  Introduction to polymer viscoelasticity , 1972 .

[51]  R. Cleland.  The Instron technique as a measure of immediate-past wall extensibility , 1984, Planta.

[52]  S. Loukin,et al.  Manganese effectively supports yeast cell-cycle progression in place of calcium , 1995, The Journal of cell biology.