Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins.

It is common for the root/shoot ratio of plants to increase when water availability is limiting. This ratio increases because roots are less sensitive than shoots to growth inhibition by low water potentials. The physiological and molecular mechanisms that assist root growth under drought conditions are reviewed, with a focus on changes in cell walls. Maize seedlings adapt to low water potential by making the walls in the apical part of the root more extensible. In part, this is accomplished by increases in expansin activity and in part by other, more complex changes in the wall. The role of xyloglucan endotransglycosylase, peroxidase and other wall enzymes in root adaptation to low water potential is evaluated and some of the complications in the field of study are listed.

[1]  R. E. Sharp,et al.  Peroxidase activity in the leaf elongation zone of tall fescue : I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. , 1992, Plant physiology.

[2]  D J Cosgrove,et al.  Wall extensibility: its nature, measurement and relationship to plant cell growth. , 1993, The New phytologist.

[3]  S. Fry Polysaccharide-Modifying Enzymes in the Plant Cell Wall , 1995 .

[4]  P. M. Neumann,et al.  The Role of Cell Wall Adjustments in Plant Resistance to Water Deficits , 1995 .

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

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

[7]  M. Evans,et al.  Cellular specifiCity of the gravitropic motor response in roots , 1997, Planta.

[8]  R. Munns Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses , 1993 .

[9]  D J Cosgrove,et al.  Enzymes and other agents that enhance cell wall extensibility. , 1999, Annual review of plant physiology and plant molecular biology.

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

[11]  A. Fleming,et al.  Analysis of expansin-induced morphogenesis on the apical meristem of tomato , 1999, Planta.

[12]  H. Seitz,et al.  Activation of cell wall-associated peroxidase isoenzymes in pea epicotyls by a xyloglucan-derived nonasaccharide , 1996 .

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

[14]  T. Flowers,et al.  Plants under stress. , 1989 .

[15]  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.

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

[17]  A. Läuchli,et al.  Changes of Cell Wall Composition and Polymer Size in Primary Roots of Cotton Seedlings Under High Salinity , 1993 .

[18]  R. E. Sharp,et al.  Spatial distribution of turgor and root growth at low water potentials. , 1991, Plant physiology.

[19]  Stephen C. Fry,et al.  Cross-Linking of Matrix Polymers in the Growing Cell Walls of Angiosperms , 1986 .

[20]  L. Taiz,et al.  Plant Cell Expansion: Regulation of Cell Wall Mechanical Properties , 1984 .

[21]  R. E. Sharp,et al.  Growth of the Maize Primary Root at Low Water Potentials : II. Role of Growth and Deposition of Hexose and Potassium in Osmotic Adjustment. , 1990, Plant physiology.

[22]  D. Cosgrove,et al.  Autolysis and extension of isolated walls from growing cucumber hypocotyls. , 1994, Journal of experimental botany.

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

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

[25]  P. Albersheim,et al.  Further studies of the ability of xyloglucan oligosaccharides to inhibit auxin-stimulated growth. , 1992, Plant physiology.

[26]  L. M. Lagrimini,et al.  Characterization of Antisense Transformed Plants Deficient in the Tobacco Anionic Peroxidase , 1997, Plant physiology.

[27]  R. E. Sharp,et al.  Growth of the maize primary root at low water potentials : I. Spatial distribution of expansive growth. , 1988, Plant physiology.

[28]  J. Pritchard,et al.  Acid-induced wall loosening is confined to the accelerating region of the root growing zone , 1999 .

[29]  T. Hsiao,et al.  Rapid Response of the Yield Threshold and Turgor Regulation during Adjustment of Root Growth to Water Stress in Zea mays , 1995, Plant physiology.

[30]  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.

[31]  M. Evans,et al.  Specialized Zones of Development in Roots , 1995, Plant physiology.

[32]  U. Kutschera The Role of the Epidermis in the Control of Elongation Growth in Stems and Coleoptiles , 1992 .

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

[34]  D W Henderson,et al.  Immediate and subsequent growth responses of maize leaves to changes in water status. , 1971, Plant physiology.

[35]  J. Boyer,et al.  Primary events regulating stem growth at low water potentials. , 1990, Plant physiology.

[36]  G. Revilla,et al.  Changes in Peroxidase Activity Associated with Cell Walls During Pine Hypocotyl Growth , 1995 .

[37]  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.

[38]  R. E. Sharp,et al.  Growth of the Maize Primary Root at Low Water Potentials : III. Role of Increased Proline Deposition in Osmotic Adjustment. , 1991, Plant physiology.

[39]  P. Navas,et al.  Role of Apoplastic and Cell-Wall Peroxidases on the Stimulation of Root Elongation by Ascorbate , 1996, Plant physiology.

[40]  P. Green Expansin and morphology: a role for biophysics , 1997 .

[41]  R. Cleland Cell Wall Extension , 1971 .

[42]  Richard C. Moore,et al.  Expansin action on cells with tip growth and diffuse growth , 1995 .

[43]  M. Probine,et al.  The Structure and Plastic Properties of the Cell Wall of Nitella in Relation to Extension Growth , 1966 .

[44]  D. Cosgrove,et al.  Acid-growth response and alpha-expansins in suspension cultures of bright yellow 2 tobacco. , 1998, Plant physiology.

[45]  W. Davies,et al.  Can cell wall peroxidase activity explain the leaf growth response of Lolium temulentum L. during drought , 1997 .

[46]  D J Cosgrove,et al.  Water Uptake by Growing Cells: An Assessment of the Controlling Roles of Wall Relaxation, Solute Uptake, and Hydraulic Conductance , 1993, International Journal of Plant Sciences.

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

[48]  J. Boyer,et al.  Turgor and growth at low water potentials. , 1989, Plant physiology.

[49]  J. Boyer Plant Productivity and Environment , 1982, Science.

[50]  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.

[51]  D. Delmer,et al.  3 – The Primary Cell Walls of Flowering Plants , 1980 .

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

[53]  R. E. Sharp,et al.  Root Growth Maintenance at Low Water Potentials (Increased Activity of Xyloglucan Endotransglycosylase and Its Possible Regulation by Abscisic Acid) , 1994, Plant physiology.

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

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

[56]  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.

[57]  G. Cramer,et al.  Kinetics of maize leaf elongation. I: Increased yield threshold limits short-term, steady-state elongation rates after exposure to salinity , 1991 .

[58]  M. Sakata,et al.  Effect of Osmotic Stress on Turgor Pressure in Mung Bean Root Cells , 1987 .

[59]  G. Cramer Kinetics of Maize Leaf Elongation : III. Silver Thiosulfate Increases the Yield Threshold of Salt-Stressed Plants, but Ethylene Is Not Involved. , 1992, Plant physiology.

[60]  J. Pritchard,et al.  Stimulation and inhibition of pine root growth by osmotic stress , 1995 .

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

[62]  R. Cleland,et al.  The Acid Growth Theory of auxin-induced cell elongation is alive and well. , 1992, Plant physiology.

[63]  J. Boyer,et al.  Inhibitory effects of water deficit on maize leaf elongation. , 1985, Plant physiology.

[64]  Jeremy Pritchard,et al.  The control of cell expansion in roots. , 1994, The New phytologist.

[65]  A. D. Tomos,et al.  Measurement of Yield Threshold and Cell Wal Extensibility of Intact Wheat Roots under Different Ionic, Osmotic and Temperature Treatments , 1990 .

[66]  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 .

[67]  R. E. Sharp,et al.  Peroxidase Activity in the Leaf Elongation Zone of Tall Fescue : II. Spatial Distribution of Apoplastic Peroxidase Activity in Genotypes Differing in Length of the Elongation Zone. , 1992, Plant physiology.

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

[69]  T. Hsiao,et al.  Transient Responses of Cell Turgor and Growth of Maize Roots as Affected by Changes in Water Potential , 1994, Plant physiology.

[70]  R. E. Sharp,et al.  Growth Maintenance of the Maize Primary Root at Low Water Potentials Involves Increases in Cell-Wall Extension Properties, Expansin Activity, and Wall Susceptibility to Expansins , 1996, Plant physiology.

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

[72]  Harry E. Ahles Hordeum vulgare L. , 1953 .

[73]  P. Albersheim,et al.  Inhibition of 2,4-dichlorophenoxyacetic Acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide. , 1984, Plant physiology.

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

[75]  P. M. Neumann,et al.  Hydraulic Signals from the Roots and Rapid Cell-Wall Hardening in Growing Maize (Zea mays L.) Leaves Are Primary Responses to Polyethylene Glycol-Induced Water Deficits , 1994, Plant physiology.

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

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

[78]  H. Griffiths,et al.  Water deficits: plant responses from cell to community. , 1993 .

[79]  L. González,et al.  Plant Water Status , 2001 .

[80]  G. Cramer,et al.  Estimation of growth parameters in salt‐stressed maize: comparison of the pressure‐block and applied‐tension techniques , 1995 .

[81]  H. Ougham,et al.  Slender barley, an extension growth mutant , 1994 .

[82]  N. Carpita STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES. , 1996, Annual review of plant physiology and plant molecular biology.

[83]  A. Showalter,et al.  Structure and function of plant cell wall proteins. , 1993, The Plant cell.

[84]  M. Evans,et al.  Kinetics of Adaptation to Osmotic Stress in Lentil (Lens culinaris Med.) Roots. , 1981, Plant physiology.

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

[86]  Peters,et al.  The Correlation of Profiles of Surface pH and Elongation Growth in Maize Roots. , 1999, Plant physiology.

[87]  R. E. Sharp,et al.  Plants under Stress: Regulation of growth and development of plants growing with a restricted supply of water , 1989 .

[88]  P. Verslues,et al.  Root growth and oxygen relations at low water potentials. Impact Of oxygen availability in polyethylene glycol solutions , 1998, Plant physiology.

[89]  N. Carpita,et al.  Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. , 1989, Plant physiology.

[90]  J. Pritchard,et al.  Biophysical and biochemical control of cell expansion in roots and leaves , 1994 .

[91]  W. Snedden,et al.  Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. , 1999, Science.

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

[93]  E. Vierling,et al.  Plant responses to environmental stress , 1992, Current Biology.

[94]  Andrew J. Fleming,et al.  Induction of Leaf Primordia by the Cell Wall Protein Expansin , 1997 .

[95]  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.