Regulation of root growth responses to water deficit

  • Eric S. Ober
  • Robert E. Sharp

Abstract

The growth and function of roots are essential for crop productivity under water-limiting conditions, but direct improvement of roots by plant breeding has been slow. One difficulty is the observation and quantitative measurement of root systems under conditions that are relevant to field environments. Another challenge is the identification of and selection for specific loci that could improve the acquisition of water from the soil profile. However, advances are being made in the understanding of root growth regulation and development. We review the evidence for the maintenance of root growth by ABA during water deficit, and the interactions with ethylene and other hormones. A biophysical model of cell expansion serves to focus discussion of topics relating to regulation of growth and development. The power of kinematic growth analysis is demonstrated by highlighting changes in growth regulatory processes and associated patterns of gene expression and protein composition that occur specifically in regions of the root where cell expansion is maintained under water deficit conditions. Growth is a complex process; new information adds further insight and further complexity to our understanding of how roots sense and respond to changes in environmental conditions. It is important to unravel these adaptive mechanisms so that it is clear how the manipulation of one process will affect the function of the whole plant, and so that the effect on final yield and water use can be predicted. This complexity makes simple linear models inadequate as explanatory tools, and a systems approach is needed to incorporate the weave of interacting networks of signaling and response pathways. The real challenge is to discover how root growth can be improved, to supply breeders with the practical tools to identify or introduce superior alleles in crop species, and ultimately to ensure that discoveries lead to improvements in productivity in the field

Keywords

Root growth water deficit ABA ethylene ROS DELLA proteins cell wall 

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References

  1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP, 2006, Integration of plant responses to environmentally activated phytohormone signals. Science 311: 91–94.PubMedGoogle Scholar
  2. Aderem A, 2005, Systems biology: its practice and challenges. Cell 121: 511–513.PubMedGoogle Scholar
  3. Baskin TI, 2000, On the constancy of cell division rate in the root meristem. Plant Molec Biol 43: 545–554.Google Scholar
  4. Bassani M, Neumann PM, Gepstein S, 2004, Differential expression profiles of growth-related genes in the elongation zone of maize primary roots. Plant Molec Biol 56: 367–380.Google Scholar
  5. Beemster GTS, Mironov V, Inzé D, 2005, Tuning the cell-cycle engine for improved plant performance. Curr. Op. Biotech. 16: 142–146.Google Scholar
  6. Bengough AG, Bransby MF, Hans J, McKenna SJ, Roberts TJ, Valentine TA, 2006, Root responses to soil physical conditions; growth dynamics from field to cell. J.Exp. Bot. 57: 437–447.PubMedGoogle Scholar
  7. Bengough AG, Gordon DC, Al-Menaie H, Ellis RP, Allan D, Keith R, Thomas WTB, Forster BP, 2004, Gel observation chamber for rapid screening of root traits in cereal seedlings. Plant Soil 262: 63–70.Google Scholar
  8. Boyer JS, 1982, Plant productivity and environment. Science 218: 443–8.PubMedGoogle Scholar
  9. Bray EA, 2004, Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J.Exp. Bot. 55: 2331–2341.PubMedGoogle Scholar
  10. Bret-Harte MS, Silk WK, 1994, Fluxes and deposition rates of solutes in growing roots of Zea mays. J. Exp. Bot. 45: 1733–42.Google Scholar
  11. Brown KF, Messem AB, Dunham RJ, Biscoe PV, 1987, Effect of drought on growth and water use of sugar beet. J. Agric. Sci. 109: 421–35.Google Scholar
  12. Cahn MD, Zobel RW, Bouldin DR, 1989, Relationship between root elongation rate and diameter and duration of growth of lateral roots of maize. Plant Soil 119: 271–279.Google Scholar
  13. Carol RJ, Dolan L, 2006, The role of reactive oxygen species in cell growth: lessons from root hairs. J. Exp. Bot. 57: 1829–1834.PubMedGoogle Scholar
  14. de Cnodder T, Vissenberg K, van der Straeten D, Verbelen JP, 2005, Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions. New Phytol. 168: 541–550.PubMedGoogle Scholar
  15. de Smet I, Zhang H, Inzé D, Beeckman T, 2006, A novel role for abscisic acid emerges from underground. Trends Plant Sci. doi:10.1016/j.tplants.2006.07.003.Google Scholar
  16. Deak KI, Malamy J, 2005, Osmotic regulation of root system architecture. Plant J. 43: 17–28.PubMedGoogle Scholar
  17. Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM, 2003, Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J. Cell Sci. 116: 81–88.PubMedGoogle Scholar
  18. Doerner P, Jorgensen J-E, You R, Steppuhn J, Lamb C, 1996, Control of root growth and development by cyclin expression. Nature 380: 520–23.PubMedGoogle Scholar
  19. Eapen D, Barroso ML, Ponce G, Campos ME, Cassab GI, 2005, Hydrotropism: root growth responses to water. Trends Plant Sci. 10:44–51.PubMedGoogle Scholar
  20. Fan L, Neumann PM, 2004, The spatially variable inhibition by water deficit of maize root growth correlates with altered profiles of proton flux and cell wall pH. Plant Physiol. 135: 1–10.Google Scholar
  21. Farrar JF, Minchin PEH, Thorpe MR, 1995, Carbon import into barley roots: effects of sugars and relation to cell expansion. J. Exp. Bot. 46: 1859–1865.Google Scholar
  22. Feijó JA, Costa SS, Prado AM, Becker JD, Certal AC, 2004, Signalling by tips. Curr. Op. Plant Biol. 7: 589–598.Google Scholar
  23. Frensch J, 1997, Primary responses of root and leaf elongation to water deficits in the atmosphere and soil solution. J. Exp. Bot. 48: 985–999.Google Scholar
  24. Frensch J, Hsiao TC, 1995, Rapid response of the yield threshold and turgor regulation during adjustment of root growth to water stress in Zea mays. Plant Physiol. 108: 303–312.PubMedGoogle Scholar
  25. Frensch J, Hsiao TC, Steudle E, 1996, Water and solute transport along developing maize roots. Planta 198: 348–55.Google Scholar
  26. Fu X, Harberd NP, 2003, Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421: 740–743.PubMedGoogle Scholar
  27. Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C, 2004, Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol. 134: 898–908.PubMedGoogle Scholar
  28. Giuliani S, Sanguinetti MC, Tuberosa R, Bellotti M, Salvi S, Landi P, 2005, Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. J. Exp. Bot. 56: 3061–3070.PubMedGoogle Scholar
  29. Gould N, Thorpe MR, Minchin PEH, Pritchard J, White PJ, 2004, Solute is imported to elongating root cells of barley as a pressure driven-flow of solution. Funct. Plant Biol. 31: 391–397.Google Scholar
  30. Grime JP, Mackey JML, 2002, The role of plasticity in resource capture by plants. Evol. Ecol. 16: 299–307.Google Scholar
  31. Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F, 2006, Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Molec. Biol. 62: 305–323.Google Scholar
  32. Hartung W, Schraut D, Jiang F, 2005, Physiology of abscisic acid (ABA) in roots under stress–a review of the relationship between root ABA and radial water and ABA flows. Aust. J. Agric. Res. 56: 1253–1259.Google Scholar
  33. Henzler T, Steudle E, 2004, Oxidative gating of water channels (aquaporins) in Chara by hydroxyl radicals. Plant Cell and Environ. 27: 1184–1195.Google Scholar
  34. Hohl M, Schopfer P, 1991, Water relations of growing maize coleoptiles. Comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressure. Plant Physiol. 95: 716–22.PubMedGoogle Scholar
  35. Hoppe DC, McCully ME, Wenzel CL, 1986, The nodal roots of Zea: their development in relation to structural features of the stem. Can. J. Bot 64: 2524–37.CrossRefGoogle Scholar
  36. Hose E, Steudle E, Hartung W, 2000, Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes. Planta 211: 874–882.PubMedGoogle Scholar
  37. Hutchings MJ, John EA, 2004, The effects of environmental heterogeneity on root growth and root/shoot partitioning. Ann. Bot. 94: 1–8.PubMedGoogle Scholar
  38. Inukai Y, Miwa M, Nagato Y, Kitano H, Yamauchi A, 2001, RRL1, RRL2 and CRL2 loci regulating root elongation in rice. Breeding Sci. 51: 231–239.Google Scholar
  39. Ito K, Tanakamaru K, Morita S, Abe J, Inanaga S, 2006, Lateral root development, including responses to soil drying, of maize (Zea mays) and wheat (Triticum aestivum) seminal roots. Physiol. Plant. 127: 260–267.Google Scholar
  40. Jacobs W.P., 1959, What substance normally controls a given biological process? I. Formulation of some rules. Devel. Biol. 1: 527–533.Google Scholar
  41. Kacperska, A, 2004, Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol. Plant. 122: 159–168.Google Scholar
  42. Kiegle E, Gilliham M, Haselhoff J, Tester M, 2000, Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J 21: 225–229.PubMedGoogle Scholar
  43. Klepper, B, 1990, Root growth and water uptake. In, Irrigation of agricultural crops, Agronomy Monograph No. 30, ASA, CSSA, SSSA, pp. 281–322.Google Scholar
  44. Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang L-F, Koch K, Fu S, Dotson A, Byers N, 2006, An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J. 46: 307–316.PubMedGoogle Scholar
  45. Kuchenbuch RO, Ingram KT, 2002, Image analysis for non-destructive and non-invasive quantification of root growth and soil water content in rhizotrons. J. of Plant Nutr. Soil Sci. 165: 573–581.Google Scholar
  46. Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI, 2003, NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22: 2623–2633.PubMedGoogle Scholar
  47. Landi P, Sanguinetti MC, Darrah LL, Giuliani MM, Salvi S, Conti S, Tuberosa R, 2002, Detection of QTLs for vertical root pulling resistance in maize and overlap with QTLs for root traits in hydroponics and for grain yield under different water regimes. Maydica 47: 233–243.Google Scholar
  48. Lee J, Das A, Yamaguchi M, Hashimoto J, Tsutsumi N, Uchimiya H, Umeda M, 2003, Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. Plant J. 34: 417–425.PubMedGoogle Scholar
  49. LeNoble ME, Spollen WG, Sharp RE, 2004, Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression. J. Exp. Bot. 55: 237–245.PubMedGoogle Scholar
  50. Lew, RR, 2004, Osmotic effects on the electrical properties of Arabidopsis root hair vacuoles in situ. Plant Physiol. 134: 352–360.PubMedGoogle Scholar
  51. Liang BM, Sharp RE, Baskin TI, 1997, Regulation of growth anisotropy in well-watered and water-stressed maize roots. I. Spatial distribution of longitudinal, radial and tangential expansion rates. Plant Physiol. 115: 101–111.PubMedGoogle Scholar
  52. Liszkay A, vander Zalm E, Schopfer P, 2004, Production of reactive oxygen intermediates (O2-, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 136: 3114–3123.PubMedGoogle Scholar
  53. Lockhart, JA, 1965, An analysis of irreversible plant cell elongation. J. Theor. Biol. 8: 264–275.PubMedGoogle Scholar
  54. Luu D-T, Maurel C, 2005, Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ. 28: 85–96.Google Scholar
  55. Lynch JP, Ho MD, 2005, Rhizoeconomics: carbon costs of phosphorous acquisition. Plant Soil 269: 45–56.Google Scholar
  56. MacRobbie, EAC, 2006, Osmotic effects on vacuolar ion release in guard cells. Proc. of the Natl. Acad. Sci. 103: 1135–1140.Google Scholar
  57. Mouchel CF, Briggs GC, Hardtke CD, 2004, Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Development 18: 700–714.PubMedGoogle Scholar
  58. Müssig C, Sin G-H, Altmann T, 2003, Brassinosteroids promote root growth in Arabidopsis. Plant Physiol. 133: 1261–1271.PubMedGoogle Scholar
  59. Ober ES, Le Bloa M, Clark CJA, Royal A, Jaggard KW, Pidgeon JD, 2005, Evaluation of physiological traits as indirect selection criteria for drought tolerance in sugar beet. Field Crops Res. 91:231–249.Google Scholar
  60. Ober ES, Sharp RE, 1994, Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. I. Requirement for increased levels of abscisic acid. Plant Physiol. 105: 981–987.PubMedGoogle Scholar
  61. Ober ES, Sharp RE, 2003, Electrophysiological responses of maize roots to low water potentials: relationship to growth and ABA accumulation. J. Exp. Bot. 54: 813–824.PubMedGoogle Scholar
  62. Osato Y, Yokoyama R, Nishitani K, 2006, A principal role for AtXTH18 in Arabidopsis thaliana root growth: a functional analysis using RNAi plants. J. Plant Res. 119: 153–162.PubMedGoogle Scholar
  63. Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA, 2005, Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc. Nat. Acad. Sci. 102:18830–18835.PubMedGoogle Scholar
  64. Passardi F, Tognolli M, De Meyer M, Penel C, Dunand C, 2006, Two cell wall associated peroxidases from Arabidopsis influence root elongation. Planta 223: 965–974.PubMedGoogle Scholar
  65. Passioura JB, 1983, Roots and drought resistance. Ag Water Manag. 7: 265–80.Google Scholar
  66. Passioura JB, 1994, The physical chemistry of the primary cell wall: implication for the control of expansion rate. J. Exp. Bot. 45: 1675–82.Google Scholar
  67. Passioura JB, 2006, Increasing crop productivity when water is scarce–from breeding to field management. Ag. Water Manag. 80: 176–196.Google Scholar
  68. Passioura JB, Boyer JS, 2003, Tissue stresses and resistance to water flow conspire to uncouple the water potential of the epidermis from that of the xylem in elongating plant stems. Funct. Plant Biol. 30: 325–334.Google Scholar
  69. Peters, WS, 2004, Growth rate gradients and extracellular pH in roots: how to control an explosion. New Phytol. 162: 571–574.Google Scholar
  70. Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ, 2006, The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci. 11: 176–183.PubMedGoogle Scholar
  71. Pierret A, Doussan C, Pagès L, 2006, Spatio-temporal variations in axial conductance of primary and first-order lateral roots of a maize crop as predicted by a model of the hydraulic architecture of root systems. Plant Soil 282: 117–126.Google Scholar
  72. Poroyko V, Spollen WG, Hejlek LG, Hernandez AG, LeNoble ME, Davis G, Nguyen HT, Springer GK, Sharp RE, Bohnert HJ, 2007, Comparing regional transcript profiles from maize primary roots under well-watered and low water potential conditions. J. Exp. Bot. 58: 279–289.PubMedGoogle Scholar
  73. Proseus TE, Boyer JS, 2006, Periplasm turgor pressure controls wall deposition and assembly in growing Chara corallina cells. Ann. Bot. 98: 93–105.PubMedGoogle Scholar
  74. Proseus TE, Zhu G-L, Boyer JS, 2000, Turgor, temperature and the growth of plant cells: using Chara corallina as a model system. J. Exp. Bot. 51: 1481–1494.PubMedGoogle Scholar
  75. Rahman A, Amakawa T, Goto N, Tsurumi S, 2001, Auxin is a positive regulator for ethylene-mediated responses in the growth of Arabidopsis roots. Plant Cell Physiol. 42: 301–307.PubMedGoogle Scholar
  76. Riefler M, Novak O, Strnad M, Schmülling T, 2006, Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40–54.PubMedGoogle Scholar
  77. Saab IN, Sharp RE, Pritchard J, 1992, Effect of inhibition of abscisic acid accumulation on the spatial distribution of elongation in the primary root and mesocotyl of maize at low water potentials. Plant Physiol. 99: 26–33.PubMedCrossRefGoogle Scholar
  78. Saab IN, Sharp RE, Pritchard J, Voetberg GS, 1990, Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol. 93: 1329–36.PubMedCrossRefGoogle Scholar
  79. Sacks M, Silk WK, Burman P, 1997, Effect of water stress on cortical cell division rates within the apical meristem of primary roots of maize. Plant Physiol. 114:519–27.PubMedGoogle Scholar
  80. Shabala SN, Lew RR, 2002, Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol. 129: 290–99.PubMedGoogle Scholar
  81. Sharp RE, 2002, Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant, Cell Environ. 25: 211–222.Google Scholar
  82. Sharp RE, Davies WJ, 1985, Root growth and water uptake by maize plants in drying soil. J. Exp. Bot. 36: 1441–56.Google Scholar
  83. Sharp RE, Hsiao TC, Silk WK, 1990, Growth of the maize primary root at low water potentials. II. Role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiol. 93: 1337–46.PubMedGoogle Scholar
  84. Sharp RE, LeNoble ME, 2002, ABA, ethylene and the control of shoot and root growth under water stress. J. Exp. Bot. 53: 33–37.PubMedGoogle Scholar
  85. Sharp RE, LeNoble ME, Else MA, Thorne ET, Gherardi F, 2000, Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. J. Exp. Bot. 51: 1575–1584.PubMedGoogle Scholar
  86. Sharp RE, Silk WK, Hsiao TC, 1988, Growth of the maize primary root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiol. 87: 50–57.PubMedGoogle Scholar
  87. Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME, 1994, Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. J Exp Bot 45: 743–51.Google Scholar
  88. Silk WK, 1984, Quantitative descriptions of development. Annu. Rev. Plant Physiol. 35: 479–518.Google Scholar
  89. Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE, 2000, ABA accumulation maintains primary root elongation at low water potentials by restricting ethylene production. Plant Physiol. 122: 967–976.PubMedGoogle Scholar
  90. Spollen WG, Sharp RE, 1991, Spatial distribution of turgor and root growth at low water potentials. Plant Physiol. 96:438–43.PubMedGoogle Scholar
  91. Spollen WG, Sharp RE, Saab IN, Wu Y, 1993, Regulation of cell expansion in roots and shoots at low water potentials. In, JAC Smith, H Griffiths, eds, Water Deficits. Plant Responses from the Cell to the Community, Bios Sci Publ, Oxford, pp 37–52.Google Scholar
  92. Steele KA, Price AH, Shashidhar HE, Witcombe JR, 2006, Marker-assisted selection to introgress rice QTLs controlling root traits into and Indian upland rice variety. Theor. Appl. Genet. 112: 208–221.PubMedGoogle Scholar
  93. Steffens B, Wang J, Sauter M, 2006, Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223: 604–612.PubMedGoogle Scholar
  94. Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR, 1997, Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. 94: 12235–40.PubMedGoogle Scholar
  95. Tsuda S, Miyamoto N, Takahashi H, Ishihara K, Hirasawa T, 2003, Roots of Pisum sativum L. exhibit hydrotropism in response to a water potential gradient in vermiculite. Ann. Bot. 92: 767–770.PubMedGoogle Scholar
  96. Ushada M, Murase H, 2006, Identification of a moss growth system using an artificial neural network model. Biosystems Engineering 94: 179–189.Google Scholar
  97. Vamerali T, Guarise M, Ganis A, Bona S, Mosca G, 2003, Analysis of root images from auger sampling with a fast procedure: a case application to sugar beet. Plant Soil 255: 387–397.Google Scholar
  98. van Beem J, Smith ME, Zobel RW, 1998, Estimating root mass in maize using a portable capacitance meter. Agron. J. 90: 566–570.CrossRefGoogle Scholar
  99. van der Weele, CM, Jiang, HS, Palaniappan, KK, Ivanov, VB, Palaniappan, K, Baskin TI, 2003, A new algorithm for computational image analysis of deformable motion at high spatial and temporal resolution applied to root growth. Roughly uniform elongation in the meristem and also, after an abrupt acceleration, in the elongation zone. . Plant Physiol. 132: 1138–1148.PubMedGoogle Scholar
  100. Vandeleur R, Miemietz C, Tilbrook J, Tyerman SD, 2005, Roles of aquaporins in root responses to irrigation. Plant Soil 274: 141–161.Google Scholar
  101. Varney GT, Canny MJ, 1993, Rates of water uptake into the mature root system of maize plants. New Phytol. 123: 775–786.Google Scholar
  102. Verslues PE, Ober ES, Sharp RE, 1998, Oxygen relations and root growth at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiol. 116: 1403–1412.PubMedGoogle Scholar
  103. Verslues PE, Sharp RE, 1999, Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiol. 119: 1349–1360.PubMedGoogle Scholar
  104. Voetberg GS, Sharp RE, 1991, Growth of the maize primary root at low waterpotentials. III. Role of increased proline depositionin osmotic adjustment. Plant Physiol 96: 1125–30.PubMedGoogle Scholar
  105. Voisin A-S, Reidy B, Parent B, Rolland G, Redondo E, Gerentes D, Tardieu F, Muller B, 2006, Are ABA, ethylene or their interaction involved in the response of leaf growth to soil water deficit? An analysis using naturally occurring variation or genetic transformation of ABA production in maize. Plant, Cell and Environ. 29: 1829–1840.Google Scholar
  106. Volkmar, KM, 1997, Water stressed nodal roots of wheat: effects on leaf growth. Aust J Plant Physiol 24: 49–56.CrossRefGoogle Scholar
  107. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG, 2006, Nitrogen regulation of root branching. Ann. Bot. 97: 875–881.PubMedGoogle Scholar
  108. Walter A, Spies H, Terjung S, Küsters R, Kirchgeβner N, Schurr U, 2002, Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing. J. Exp. Bot. 53: 689–698.PubMedGoogle Scholar
  109. Watt M, Silk WK, Passioura JB, 2006, Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Ann. Bot. 97: 839–855.PubMedGoogle Scholar
  110. Weaver, JE, 1926, Root habits of corn or maize. Root development of field crops, McGraw Hill, New York, pp 180–191.Google Scholar
  111. Weih, M, 2003, Trade-offs in plants and the prospects for breeding using modern biotechnology. New Phytol 158:1–9.Google Scholar
  112. Wenzel CL, McCully ME, Canny MJ, 1989, Development of water conducting capacity in the root systems of young plants of corn and some other C4grasses. Plant Physiol. 89: 1094–1101.PubMedGoogle Scholar
  113. Whalley WR, Clark LJ, Gowing DJG, Cope RE, Lodge RE, Leeds-Harrison PB, 2006, Does soil strength play a role in wheat yield losses caused by soil drying? Plant Soil 280: 279–290.Google Scholar
  114. Wojtaszek P, Anielska-Mazur A, Gabrys H, Baluska F, Volkmann D, 2005, Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing. Funct. Plant Biol. 32: 721–736.Google Scholar
  115. Wu Y, Sharp RE, Durachko DM, Cosgrove DJ, 1996, 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. Plant Physiol 111: 765–772.PubMedGoogle Scholar
  116. Wu Y, Spollen WG, Sharp RE, Hetherington PR, Fry SC, 1994, Root growth maintenance at low water potentials. Increased activity of xyloglucan endotransglycosylase and its possible regulation by ABA. Plant Physiol 106: 607–615.PubMedGoogle Scholar
  117. Wu Y, Thorne ET, Sharp RE, Cosgrove DJ, 2001, Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiol. 126: 1471–1479.PubMedGoogle Scholar
  118. Yang Z, Tian LN, Latoszek-Green M, Brown D, Wu KQ, 2005, Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molec. Biol. 58: 585–596.Google Scholar
  119. Yim HH, Villarejo MR, 1994, Gene expression and osmoregulation in bacteria. In, K. Strange, ed, Cellular and Molecular Physiology of Cell Volume Regulation, CRC Press, Boca Raton, Fla, pp 334–46.Google Scholar
  120. Zhu J, Chen S, Alvarez S, Asirvatham VS, Schachtman DP, Wu Y, Sharp RE, 2006, Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol. 140: 311–325.PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Eric S. Ober
    • 1
  • Robert E. Sharp
    • 2
  1. 1.Rothamsted ResearchBroom’s Barn Research StationHighamUK
  2. 2.Division of Plant SciencesUniversity of MissouriColumbiaUSA

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