Long-Distance Signals Produced by Water-Stressed Roots

  • Jason Q. D. Goodger
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 19)


Roots can sense small changes in soil water status and rapidly communicate this over long distances throughout the plant. This sets in motion numerous response mechanisms for water conservation and drought tolerance, largely facilitated by the hormone ABA. Despite impressive advances in the molecular mechanisms by which ABA mediates such plant responses, long-distance signaling of soil water status remains relatively poorly understood. Recent results refute the long-held hypothesis of ABA biosynthesis in roots as the primary signal, at least in the initial stage of water stress communication. This chapter examines the involvement of leaf ABA biosynthesis, pH-mediated ABA redistribution, and ABA conjugate catabolism in communicating soil water status. In addition, the chapter presents current knowledge on other xylem-borne signaling compounds such as cytokinins, 1-aminocyclopropane-1-carboxylic acid, inorganic ions, and organic acids and their possible interactions with ABA in long-distance signaling of water stress.


Water Stress Guard Cell Stomatal Closure Soil Water Potential Plant Water Status 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was funded by a grant from the Australian Research Council (Project DP1094530).


  1. Acharya B, Assmann S (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462PubMedCrossRefGoogle Scholar
  2. Alvarez S, Goodger JQD, Marsh EL, Chen SX, Asirvatham VS, Schachtman DP (2006) Characterization of the maize xylem sap proteome. J Proteome Res 5:963–972PubMedCrossRefGoogle Scholar
  3. Alvarez S, Marsh EL, Schroeder SG, Schachtman DP (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31:325–340PubMedCrossRefGoogle Scholar
  4. Bacon MA, Wilkinson S, Davies WJ (1998) pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent. Plant Physiol 118:1507–1515PubMedCrossRefGoogle Scholar
  5. Bahrun A, Jensen CR, Asch F, Mogensen VO (2002) Drought-induced changes in xylem pH, ionic composition, and ABA concentration act as early signals in field-grown maize (Zea mays L.). J Exp Bot 53:251–263PubMedCrossRefGoogle Scholar
  6. Ben-Ari G (2012) The ABA signal transduction mechanism in commercial crops: learning from Arabidopsis. Plant Cell Rep 31:1357–1369PubMedCrossRefGoogle Scholar
  7. Biles CL, Abeles FB (1991) Xylem sap proteins. Plant Physiol 96:597–601PubMedCrossRefGoogle Scholar
  8. Blackman PG, Davies WJ (1985) Root to shoot communication in maize plants of the effects of soil drying. J Exp Bot 36:39–48CrossRefGoogle Scholar
  9. Bogoslavsky L, Neumann PM (1998) Rapid regulation by acid pH of cell wall adjustment and leaf growth in maize plants responding to reversal of water stress. Plant Physiol 118:701–709PubMedCrossRefGoogle Scholar
  10. Borel C, Frey A, Marion-Poll A, Tardieu F, Simonneau T (2001) Does engineering abscisic acid biosynthesis in Nicotiana plumbaginifolia modify stomatal response to drought? Plant Cell Environ 24:477–489CrossRefGoogle Scholar
  11. Boyer JS, Westgate ME (2004) Grain yields with limited water. J Exp Bot 55:2385–2394PubMedCrossRefGoogle Scholar
  12. Brugiere N, Jiao SP, Hantke S, Zinselmeier C, Roessler JA, Niu XM, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240PubMedCrossRefGoogle Scholar
  13. Buhtz A, Kolasa A, Arlt K, Walz C, Kehr J (2004) Xylem sap protein composition is conserved among different plant species. Planta 219:610–618PubMedCrossRefGoogle Scholar
  14. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749PubMedCrossRefGoogle Scholar
  15. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  16. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell Environ 14:2723–2743CrossRefGoogle Scholar
  17. Christmann A, Hoffmann T, Teplova I, Grill E, Muller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 137:209–219PubMedCrossRefGoogle Scholar
  18. Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174PubMedCrossRefGoogle Scholar
  19. Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol Plant Mol Biol 42:55–76CrossRefGoogle Scholar
  20. Davies WJ, Wilkinson S, Loveys BR (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytol 153:449–460CrossRefGoogle Scholar
  21. Davies WJ, Kudoyarova GR, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285–295CrossRefGoogle Scholar
  22. Desikan R, Last K, Harrett-Williams R, Taglavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916PubMedCrossRefGoogle Scholar
  23. Dietz KJ, Sauter A, Wichert K, Messdaghi D, Hartung W (2000) Extracellular beta-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. J Exp Bot 51:937–944PubMedCrossRefGoogle Scholar
  24. Dodd IC, Tan LP, He J (2003) Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation? J Exp Bot 54:1281–1288PubMedCrossRefGoogle Scholar
  25. Dry PR, Loveys BR (1999) Grapevine shoot growth and stomatal conductance are reduced when part of the root system is dried. Vitis 38:151–156Google Scholar
  26. Else MA, Jackson MB (1998) Transport of 1-aminocyclopropane-1-carboxylic acid (ACC) in the transpiration stream of tomato (Lycopersicon esculentum) in relation to foliar ethylene production and petiole epinasty. Aust J Plant Physiol 25:453–458CrossRefGoogle Scholar
  27. Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993PubMedCrossRefGoogle Scholar
  28. Ernst L, Goodger JQD, Alvarez S, Marsh EL, Berla B, Lockhart E, Jung J, Li P, Bohnert HJ, Schachtman DP (2010) Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. J Exp Bot 61:3395–3405PubMedCrossRefGoogle Scholar
  29. Freundl E, Steudle E, Hartung W (2000) Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis. Planta 210:222–231PubMedCrossRefGoogle Scholar
  30. Gollan T, Schurr U, Schulze E-D (1992) Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annus. I. The concentration of cations, anions, amino acids in, and pH of, the xylem sap. Plant Cell Environ 15:551–559CrossRefGoogle Scholar
  31. Goodger JQD, Schachtman DP (2010a) Nitrogen source influences root to shoot signaling under drought. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer Science, Dordrecht, pp 165–173Google Scholar
  32. Goodger JQD, Schachtman DP (2010b) Re-examining the role of ABA as the primary long-distance signal produced by water-stressed roots. Plant Signal Behav 5:1298–1301PubMedCrossRefGoogle Scholar
  33. Goodger JQD, Sharp RE, Marsh EL, Schachtman DP (2005) Relationships between xylem sap constituents and leaf conductance of well-watered and water-stressed maize across three xylem sap sampling techniques. J Exp Bot 56:2389–2400PubMedCrossRefGoogle Scholar
  34. Hansen H, Dörffling K (1999) Changes of free and conjugated abscisic acid and phaseic acid in xylem sap of drought-stressed sunflower plants. J Exp Bot 50:1599–1605Google Scholar
  35. Hansen H, Dörffling K (2003) Root-derived trans-zeatin riboside and abscisic acid in drought-stressed and rewatered sunflower plants: interaction in the control of leaf diffusive resistance? Funct Plant Biol 30:365–375CrossRefGoogle Scholar
  36. Hartung W, Wilkinson S, Davies WJ (1998) Factors that regulate abscisic acid concentrations at the primary site of action at the guard cell. J Exp Bot 49:361–367Google Scholar
  37. Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355PubMedCrossRefGoogle Scholar
  38. Hedrich R, Marten I, Lohse G, Dietrich P, Winter H, Lohaus G, Heldt H-W (1994) Malate-sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration. Plant J 6:741–748CrossRefGoogle Scholar
  39. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052PubMedCrossRefGoogle Scholar
  40. Holbrook NM, Shashidhar VR, James RA, Munns R (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 53:1503–1514PubMedCrossRefGoogle Scholar
  41. Hose E, Steudle E, Hartung W (2000) Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes. Planta 211:874–882PubMedCrossRefGoogle Scholar
  42. Ikegami K, Okamoto M, Seo M, Koshiba T (2009) Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit. J Plant Res 122:235–243PubMedCrossRefGoogle Scholar
  43. Jia W, Davies WJ (2007) Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced abscisic acid signals. Plant Physiol 143:68–77PubMedCrossRefGoogle Scholar
  44. Jia W, Zhang J (2008) Stomatal movements and long-distance signaling in plants. Plant Signal Behav 3:772–777PubMedCrossRefGoogle Scholar
  45. Jia W, Liang J, Zhang J (2001) Initiation and regulation of water deficit-induced abscisic acid accumulation in maize leaves and roots: cellular volume and water relations. J Exp Bot 52:295–300PubMedCrossRefGoogle Scholar
  46. Jones RJ, Mansfield TA (1971) Antitranspirant activity of the methyl and phenyl esters of abscisic acid. Nature 231:331–332PubMedCrossRefGoogle Scholar
  47. Kaiser WM, Hartung W (1981) Uptake and release of abscisic acid by isolated photoautotrophic mesophyll cells, depending on pH gradients. Plant Physiol 68:202–206PubMedCrossRefGoogle Scholar
  48. Kehr J, Buhtz A, Giavalisco P (2005) Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol 5:11PubMedCrossRefGoogle Scholar
  49. Kharin VV, Zwiers FW, Zhang X, Hegerl GC (2007) Changes in temperature and precipitation extremes in the IPCC ensemble of global coupled model simulations. J Clim 20:1419–1444CrossRefGoogle Scholar
  50. Klingler JP, Batelli G, Zhu J-K (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199–3210PubMedCrossRefGoogle Scholar
  51. Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134:1697–1707PubMedCrossRefGoogle Scholar
  52. Kondo N, Sugahara K (1978) Changes in transpiration rate of SO2-resistant and -sensitive plants with SO2 fumigation and the participation of abscisic acid. Plant Cell Physiol 19:365–373Google Scholar
  53. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced rearrangements and regulatory networks. J Exp Bot 63:1593–1608PubMedCrossRefGoogle Scholar
  54. Krishnan HB, Natarajan SS, Bennett JO, Sicher RC (2011) Protein and metabolite composition of xylem sap from field-grown soybeans (Glycine max). Planta 233:921–931PubMedCrossRefGoogle Scholar
  55. Kudoyarova GR, Vysotskaya LB, Cherkozyanova A, Dodd IC (2007) Effect of partial rootzone drying on the concentration of zeatin-like cytokinins in tomato (Solanum lycopersicum L.) xylem sap and leaves. J Exp Bot 58:161–168PubMedCrossRefGoogle Scholar
  56. Kudoyarova G, Veselova S, Hartung W, Farkhutdinov RG, Veselov DS, Sharipova G (2011) Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporative demand. Planta 233:87–94PubMedCrossRefGoogle Scholar
  57. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120PubMedCrossRefGoogle Scholar
  58. Li S, Assmann SM, Albert R (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312PubMedCrossRefGoogle Scholar
  59. Liang J, Zhang J (1997) Collection of xylem sap at flow rate similar to in vivo transpiration flux. Plant Cell Physiol 38:1375–1381CrossRefGoogle Scholar
  60. Ligat L, Lauber E, Albenne C, San Clemente H, Valot B, Zivy M, Pont-Lezica R, Arlat M, Jamet E (2011) Analysis of the xylem sap proteome of Brassica oleracea reveals a high content in secreted proteins. Proteomics 11:1798–1813PubMedCrossRefGoogle Scholar
  61. Lindsey K, Casson S, Chilley P (2002) Peptides: new signalling molecules in plants. Trends Plant Sci 7:78–83PubMedCrossRefGoogle Scholar
  62. Liu L, McDonald AJS, Stadenberg I, Davies WJ (2001) Stomatal and leaf growth responses to partial drying of root tips in willow. Tree Physiol 21:765–770PubMedCrossRefGoogle Scholar
  63. Liu FL, Jensen CR, Andersen MN (2003) Hydraulic and chemical signals in the control of leaf expansion and stomatal conductance in soybean exposed to drought stress. Funct Plant Biol 30:65–73CrossRefGoogle Scholar
  64. Liu F, Jensen CR, Andersen MN (2005) A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Aust J Agric Res 56:1245–1252CrossRefGoogle Scholar
  65. Loveys BR (1977) The intracellular location of abscisic acid in stressed and non-stressed leaf tissue. Physiol Plant 40:6–10CrossRefGoogle Scholar
  66. Lü B, Chen F, Gong ZH, Xie H, Zhang JH, Liang JS (2007) Intracellular localization of integrin-like protein and its roles in osmotic stress-induced abscisic acid biosynthesis in Zea mays. Protoplasma 232:35–43PubMedCrossRefGoogle Scholar
  67. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  68. Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–51CrossRefGoogle Scholar
  69. Mosquna A, Peterson FC, Park SY, Lozano-Juste J, Volkman BF, Cutler SR (2011) Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist-bound conformation. Proc Natl Acad Sci USA 108:20838–20843PubMedCrossRefGoogle Scholar
  70. Munns R, King RW (1988) Abscisic acid is not the only stomatal inhibitor in the transpiration stream of wheat plants. Plant Physiol 88:703–708PubMedCrossRefGoogle Scholar
  71. Munns R, Passioura JB, Milborrow BV, James RA, Close TJ (1993) Stored xylem sap from wheat and barley in drying soil contains a transpiration inhibitor with a large molecular size. Plant Cell Environ 16:867–872CrossRefGoogle Scholar
  72. Neumann PM (2007) Evidence for long distance xylem transport of signal peptide activity from tomato roots. J Exp Bot 58:2217–2223PubMedCrossRefGoogle Scholar
  73. Neumann PM (2008) Coping mechanisms for crop plants in drought-prone environments. Ann Bot 101:901–907PubMedCrossRefGoogle Scholar
  74. Neumann PM, Chazen O, Bogoslavsky L, Hartung W (1997) Role of root derived ABA in regulating early leaf growth responses to water deficits. In: Altman A, Waisel Y (eds) Biology of root formation and development. Plenum, New York, pp 147–154CrossRefGoogle Scholar
  75. Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomis C, Cutler SR, Schroeder JI, Getzoff ED (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326:1373–1379PubMedCrossRefGoogle Scholar
  76. Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149:2000–2012PubMedCrossRefGoogle Scholar
  77. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodrigues PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutter SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedGoogle Scholar
  78. Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83CrossRefGoogle Scholar
  79. Patonnier M, Peltier J, Marigo G (1999) Drought-induced increase in xylem malate and mannitol concentrations and closure of Fraxinus excelsior L. stomata. J Exp Bot 50:1223–1231Google Scholar
  80. Peterlunger E, Maragoni B, Testolin R, Vizzotto G, Costa G (1990) Carbohydrates, organic acids and mineral elements in xylem sap bleeding from kiwifruit canes. Acta Hortic 282:273–282Google Scholar
  81. Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183PubMedCrossRefGoogle Scholar
  82. Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross AR, Abrams SR, Bowles DJ (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46:492–502PubMedCrossRefGoogle Scholar
  83. Prokic LJ, Jovanovic Z, McAinsh MR, Vucinic Z, Stikic R (2006) Species-dependent changes in stomatal sensitivity to abscisic acid mediated by external pH. J Exp Bot 57:675–683PubMedCrossRefGoogle Scholar
  84. Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361PubMedCrossRefGoogle Scholar
  85. Radin JW, Parker LL, Guinn G (1982) Water relations of cotton plants under nitrogen deficiency. V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiol 70:1066–1070PubMedCrossRefGoogle Scholar
  86. Rajala A, Peltonen-Sainio P (2001) Plant growth regulator effects on spring cereal root and shoot growth. Agron J 93:936–943CrossRefGoogle Scholar
  87. Reinoso H, Sosa L, Reginato M, Luna V (2005) Histological alterations induced by sodium sulfate in the vegetative anatomy of Prosopis strombulifera (Lam.) Benth. World J Agric Sci 1:109–119Google Scholar
  88. Ren Y, Chen L, Zhang Y, Kang X, Zhang Z, Wang Y (2012) Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Funct Integr Genomics 12:327–339PubMedCrossRefGoogle Scholar
  89. Ryan CA, Pearce G, Scheer J, Moura DS (2002) Polypeptide hormones. Plant Cell 14:S251–S264PubMedGoogle Scholar
  90. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449PubMedCrossRefGoogle Scholar
  91. Santiago J, Dupeux F, Betz K, Antoni R, Gonzalez-Guzman M, Rodriguez L, Marquez JA, Rodriguez PL (2012) Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci 182:3–11PubMedCrossRefGoogle Scholar
  92. Sauter A, Hartung W (2000) Radial transport of abscisic acid conjugates in maize roots: its implication for long distance stress signals. J Exp Bot 51:929–935PubMedCrossRefGoogle Scholar
  93. Sauter A, Hartung W (2002) The contribution of internode and mesocotyl tissues to root-to-shoot signalling of abscisic acid. J Exp Bot 53:297–302PubMedCrossRefGoogle Scholar
  94. Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287PubMedCrossRefGoogle Scholar
  95. Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69PubMedCrossRefGoogle Scholar
  96. Scheible WR, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798PubMedGoogle Scholar
  97. Schell J (1997) Interdependence of pH, malate concentration, and calcium and magnesium concentrations in the xylem sap of beech roots. Tree Physiol 17:479–483PubMedCrossRefGoogle Scholar
  98. Schraut D, Heilmeier H, Hartung W (2005) Radial transport of water and abscisic acid (ABA) in roots of Zea mays under conditions of nutrient deficiency. J Exp Bot 56:879–886PubMedCrossRefGoogle Scholar
  99. Senden MHMN, Van der Meer AJGM, Limborgh J, Wolterbeek HT (1992) Analysis of major tomato xylem organic acids and PITC-derivatives of amino acids by RP-HPLC and UV detection. Plant Soil 142:81–89Google Scholar
  100. Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot responses to water stress. Plant Cell Environ 25:211–222PubMedCrossRefGoogle Scholar
  101. Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351PubMedCrossRefGoogle Scholar
  102. Sheard LB, Zheng N (2009) Signal advance for abscisic acid. Nature 462:575–576PubMedCrossRefGoogle Scholar
  103. Sobeih W, Dodd IC, Bacon MA, Grierson DC, Davies WJ (2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial rootzone drying. J Exp Bot 55:2353–2364PubMedCrossRefGoogle Scholar
  104. Song X, She X, Zhang B (2008) Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiol Plant 132:514–525PubMedCrossRefGoogle Scholar
  105. Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol 122:967–976PubMedCrossRefGoogle Scholar
  106. Stoll M, Loveys BR, Dry PR (2000) Hormonal changes induced by partial rootzone drying of irrigated grapevine. J Exp Bot 51:1627–1634PubMedCrossRefGoogle Scholar
  107. Sunkar R, Chinnusamy V, Zhu J, Zhu J-K (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309PubMedCrossRefGoogle Scholar
  108. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343PubMedCrossRefGoogle Scholar
  109. Tardieu F, Parent B, Simonneau T (2010) Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant Cell Environ 33:636–647PubMedCrossRefGoogle Scholar
  110. Teplova I, Farkhutdinov RG, Mitrichenko AN, Ivanov II, Veselov SY, Valcke RL, Kudoyarova GR (2000) Response of tobacco plants transformed with the ipt gene to elevated temperature. Russ J Plant Physl 47:367–369Google Scholar
  111. Thompson AJ, Mulholland BJ, Jackson AC, McKee JMT, Hilton HW, Symonds RC, Sonneveld T, Burbidge A, Stevenson P, Taylor IB (2007) Regulation and manipulation of ABA biosynthesis in roots. Plant Cell Environ 30:67–78PubMedCrossRefGoogle Scholar
  112. Tiekstra AE, Else MA, Jackson MB (2000) External pressures based on leaf water potentials do not induce xylem sap flow at rates of whole plant transpiration from roots of flooded or well-drained tomato and maize plants. Impact of shoot hydraulic resistances. Ann Bot 86:665–674CrossRefGoogle Scholar
  113. Vartanian N, Marcotte L, Giraudat J (1994) Drought rhizogenesis in Arabidopsis thaliana (differential responses of hormonal mutants). Plant Physiol 104:761–767PubMedGoogle Scholar
  114. Vysotskaya LB, Kudoyarova GR, Veselov SY, Jones HG (2004) Effect of partial root excision on transpiration, root hydraulic conductance and leaf growth in wheat seedlings. Plant Cell Environ 27:69–77CrossRefGoogle Scholar
  115. Vysotskaya LB, Korobova AV, Veselov SY, Dodd IC, Kudoyarova GR (2009) ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat. Funct Plant Biol 36:66–72CrossRefGoogle Scholar
  116. Vysotskaya LB, Wilkinson S, Davies WJ, Arkhipova TN, Kudoyarova GR (2011) The effect of competition from neighbours on stomatal conductance in lettuce and tomato plants. Plant Cell Environ 34:729–737PubMedCrossRefGoogle Scholar
  117. Walton DC, Harrison MA, Cote P (1976) The effects of water stress on abscisic acid levels and metabolism in roots of Phaseolus vulgaris and other plants. Planta 131:141–144CrossRefGoogle Scholar
  118. Wilkinson S (1999) pH as a stress signal. Plant Growth Regul 29:87–99CrossRefGoogle Scholar
  119. Wilkinson S (2004) Water use efficiency and chemical signalling. In: Bacon MA (ed) Water use efficiency in plant biology. Blackwell, Oxford, pp 75–112Google Scholar
  120. Wilkinson S, Davies WJ (1997) Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 113:559–573PubMedGoogle Scholar
  121. Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210PubMedCrossRefGoogle Scholar
  122. Wilkinson S, Davies WJ (2009) Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. Plant Cell Environ 32:949–959PubMedCrossRefGoogle Scholar
  123. Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525PubMedCrossRefGoogle Scholar
  124. Wilkinson S, Corlett JE, Oger L (1998) Effects of xylem pH on transpiration from wild-type and flacca tomato leaves: a vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiol 117:703–709PubMedCrossRefGoogle Scholar
  125. Wilkinson S, Bacon MA, Davies WJ (2007) Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and xylem sap pH in maize. J Exp Bot 58:1705–1716PubMedCrossRefGoogle Scholar
  126. Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509PubMedCrossRefGoogle Scholar
  127. Zeevart JAD, Boyer GJ (1984) Accumulation and transport of abscisic acid and its metabolites in Ricinus and Xanthium. Plant Physiol 74:934–939CrossRefGoogle Scholar
  128. Zhang J, Davies WJ (1989) Abscisic acid produced in dehydrating roots may enable the plant to measure the water status of the soil. Plant Cell Environ 12:73–81CrossRefGoogle Scholar
  129. Zhang J, Tardieu F (1996) Relative contribution of apices and mature tissues to ABA synthesis in droughted maize root systems. Plant Cell Physiol 37:598–605CrossRefGoogle Scholar
  130. Zhang J, Schurr U, Davies WJ (1987) Control of stomatal behaviour by abscisic acid which apparently originates in the roots. J Exp Bot 38:1174–1181CrossRefGoogle Scholar
  131. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.School of BotanyThe University of MelbourneParkvilleAustralia

Personalised recommendations