, Volume 161, Issue 1, pp 15–24 | Cite as

The importance of nutritional regulation of plant water flux

  • Michael D. CramerEmail author
  • Heidi-Jayne Hawkins
  • G. Anthony Verboom
Concepts, Reviews and Syntheses


Transpiration is generally considered a wasteful but unavoidable consequence of photosynthesis, occurring because water is lost when stomata open for CO2 uptake. Additionally, transpiration has been ascribed the functions of cooling leaves, driving root to shoot xylem transport and mass flow of nutrients through the soil to the rhizosphere. As a consequence of the link between nutrient mass flow and transpiration, nutrient availability, particularly that of NO3 , partially regulates plant water flux. Nutrient regulation of transpiration may function through the concerted regulation of: (1) root hydraulic conductance through control of aquaporins by NO3 , (2) shoot stomatal conductance (g s) through NO production, and (3) pH and phytohormone regulation of g s. These mechanisms result in biphasic responses of water flux to NO3 availability. The consequent trade-off between water and nutrient flux has important implications for understanding plant distributions, for production of water use-efficient crops and for understanding the consequences of global-change-linked CO2 suppression of transpiration for plant nutrient acquisition.


Agriculture Elevated carbon dioxide Leaf size Nocturnal transpiration Water use efficiency 



Funding was from the University of Cape Town URC awards, National Research Foundation and Protea Producers of South Africa. We are grateful for useful comments from the anonymous reviewers.


  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedGoogle Scholar
  2. Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9:511–519Google Scholar
  3. Asseng S, Turner NC, Keating BA (2001) Analysis of water- and nitrogen-use efficiency of wheat in a Mediterranean climate. Plant Soil 233:127–143Google Scholar
  4. Barber SA (1962) A diffusion and mass-flow concept of soil nutrient availability. Soil Sci 93:39–49Google Scholar
  5. Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach, 2nd edn. Wiley, New YorkGoogle Scholar
  6. Barber SA, Ozanne OG (1970) Autoradiographic evidence for the differential effect of four plants species in altering the calcium content of the rhizosphere soil. Soil Sci Soc Am Proc 34:635–637Google Scholar
  7. Bloom AJ, Meyerhoff PA, Taylor AR, Rost TL (2003) Root development and absorption of ammonium and nitrate from the rhizosphere. J Plant Growth Regul 21:416–431Google Scholar
  8. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898PubMedGoogle Scholar
  9. Caird MA, Richards JH, Donovan LA (2007) Night-time stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol 143:4–10PubMedGoogle Scholar
  10. Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199:372–381Google Scholar
  11. Cechin I, Fumis TD (2004) Effect of nitrogen supply on growth and photosynthesis of sunflower plants grown in the greenhouse. Plant Sci 166:1379–1385Google Scholar
  12. Chaillou S, Lamaze T (2001) Ammoniacal nutrition of plants. In: Morot-Gaudry J-F (ed) Nitrogen assimilation by plants. Science Publishers, NH, pp 53–69Google Scholar
  13. Chapin FSIII, Walter CHS, Clarkson DT (1988) Growth response of barley and tomato to nitrogen stress and its control by abscisic acid, water relations and photosynthesis. Planta 173:352–366Google Scholar
  14. Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764PubMedGoogle Scholar
  15. Chaves MM, Osório J, Pereira JS (2004) Water use efficiency and photosynthesis. In: Bacon MS (ed) Water use efficiency in plant biology. Blackwell, OxfordGoogle Scholar
  16. Ciompi S, Gentili E, Guidi L, Soldanti GF (1996) The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. Plant Sci 118:177–184Google Scholar
  17. Clarkson DT (1981) Nutrient interception and transport by root systems. In: Johnson CB (ed) Physiological factors limiting plant productivity. Butterworths, London, pp 307–314Google Scholar
  18. Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70PubMedGoogle Scholar
  19. Cochard H, Venisse J-S, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143:122–133PubMedGoogle Scholar
  20. Colmer TD, Bloom AJ (1998) A comparison of NH4 + and NO3 net fluxes along roots of rice and maize. Plant Cell Environ 21:240–246Google Scholar
  21. Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460PubMedGoogle Scholar
  22. Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiol Plant 89:570–576Google Scholar
  23. Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Chang Biol 4:43–54Google Scholar
  24. Cowan IR (1977) Stomatal behavior and environment. Adv Bot Res 4:117–228Google Scholar
  25. Cramer MD, Hawkins H-J (2009) A physiological mechanism for the formation of root casts. Palaeogeogr Palaeoclimatol Palaeoecol 274:125–133Google Scholar
  26. Cramer MD, Lewis OAM (1993) The influence of NO3 and NH4 + nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants. Ann Bot 72:359–365Google Scholar
  27. Cramer MD, Hoffmann V, Verboom GA (2008) Nutrient availability moderates transpiration in Ehrharta calycina. New Phytol 179:1048–1057PubMedGoogle Scholar
  28. Daley MJ, Phillips NG (2006) Interspecific variation in night-time transpiration and stomatal conductance in a mixed New England deciduous forest. Tree Physiol 26:411–419PubMedGoogle Scholar
  29. Darwin F (1898) Observations on stomata. Proc R Soc Lond 63:413–417Google Scholar
  30. Dawson TE, Burgess SSO, Tu KP, Oliveira RS, Santiago LS, Fisher JB, Simonin KA, Ambrose AR (2007) Night-time transpiration in woody plants from contrasting ecosystems. Tree Physiol 27:561–575PubMedGoogle Scholar
  31. Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318PubMedGoogle Scholar
  32. Epstein E, Bloom AJ (eds) (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer, SunderlandGoogle Scholar
  33. Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fenn 36:625–637Google Scholar
  34. Field C, Merino J, Mooney HA (1983) Compromises between water-use efficiency and nitrogen-use efficiency in five species of California evergreens. Oecologia 60:384–389Google Scholar
  35. Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmésl J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621PubMedGoogle Scholar
  36. Foyer CH, Chaumont M, Murchie E, Galtier N, Ferrario S (1995) End-product modulation of carbon partitioning with a view to improved biomass production. In: Madore MA, Lucas WJ (eds) Carbon partitioning and source–sinks interactions in plants. American Society of Plant Physiologists, Rockville, pp 45–55Google Scholar
  37. Fredeen AL, Gamon JA, Field CB (1991) Responses of photosynthesis and carbohydrate-partitioning to limitation in nitrogen and water availability in field-grown sunflower. Plant Cell Environ 14:963–970Google Scholar
  38. Gloser V, Zwieniecki MA, Orians CM, Holbrook NM (2007) Dynamic changes in root hydraulic properties in response to nitrate availability. J Exp Bot 58:2409–2415PubMedGoogle Scholar
  39. Gorska A, Ye Q, Holbrook NM, Zwieniecki MA (2008) Nitrate control of root hydraulic properties in plants: translating local information to whole plant response. Plant Physiol 148:1159–1167PubMedGoogle Scholar
  40. Greenwood DJ, Karpinets TV (1997) Dynamic model for the effects of K-fertilizer on crop growth, K-uptake and soil-K in arable cropping. 1. Description of the model. Soil Use Manage 13:178–183Google Scholar
  41. Gregory PJ (2004) Agronomic approaches to increasing water use efficiency. In: Bacon MA (ed) Water use efficiency in plant biology. Blackwell, Oxford, pp 142–170Google Scholar
  42. Guo S, Kaldenhoff R, Uehlein N, Sattelmacher B, Brueck H (2007a) Relationship between water and nitrogen uptake in nitrate- and ammonium-supplied Phaseolus vulgaris L. plants. J Plant Nutr Soil Sci 170:73–80Google Scholar
  43. Guo S, Shen O, Brueck H (2007b) Effects of local nitrogen supply on water uptake of bean plants in a split root system. J Integr Plant Biol 49:472–480Google Scholar
  44. Haberl H, Erb KH, Krausmann F, Gaube V, Bondeau A, Plutzar C, Gingrich S, Lucht W, Fischer-Kowalski M (2007) Quantifying and mapping the human appropriation of net primary production in earth’s terrestrial ecosystems. Proc Natl Acad Sci USA 104:12942–12947PubMedGoogle Scholar
  45. Hachez C, Moshelion M, Zelazny E, Cavezl 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. J Plant Mol Biol 62:305–323Google Scholar
  46. Hamdy A, Ragab R, Scarascia-Mugnozza E (2003) Coping with water scarcity: water saving and increasing water productivity. Irrig Drain 52:3–20Google Scholar
  47. Hawkins H-J, Lewis OAM (1993) Combination effect of NaCl Salinity, nitrogen form and calcium concentration on the growth, ionic content and gaseous exchange properties of Triticum aestivum L. cv. Gamtoos. New Phytol 124:161–170Google Scholar
  48. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedGoogle Scholar
  49. Ho LC (1992) The possible effects of sink demand for assimilate on photosynthesis. In: Murata N (ed) Research in photosynthesis, vol IV. Kluwer, Dordrecht, pp 729–736Google Scholar
  50. Hoffland E, Bloemhof HS, Leffelaar PA, Findenegg GR, Nelemans JA (1990) Simulation of nutrient uptake by a growing root system considering increasing root density and inter-root competition. Plant Soil 1124:149–155Google Scholar
  51. Howard AR, Donovan LA (2007) Helianthus night-time conductance and transpiration respond to soil water but not nutrient availability. Plant Physiol 143:145–155PubMedGoogle Scholar
  52. Jackson LE, Bloom AJ (1990) Root distribution in relation to soil nitrogen availability in field-grown tomatoes. Plant Soil 128:115–126Google Scholar
  53. Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower; maize and wheat plants. J Exp Bot 42:1003–1011Google Scholar
  54. Javot H, Christophe M (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–313PubMedGoogle Scholar
  55. Jia W, Davies WJ (2007) Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced ABA signals. Plant Physiol 143:68–77PubMedGoogle Scholar
  56. Jones HG (1992) Plants and microclimate: a quantitative approach to environmental plant physiology, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  57. Kage H (1997) Is low rooting density of faba beans a cause of high residual nitrate content of soil at harvest? Plant Soil 190:47–60Google Scholar
  58. Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiol 187:169–176Google Scholar
  59. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Mol Biol 47:509–540Google Scholar
  60. Kolla VA, Raghavendra AS (2007) Nitric oxide is a signaling intermediate during bicarbonate-induced stomatal closure in Pisum sativum. Physiol Plant 130:91–98Google Scholar
  61. Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619Google Scholar
  62. Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411PubMedGoogle Scholar
  63. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San DiegoGoogle Scholar
  64. Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology. Springer, New YorkGoogle Scholar
  65. Lamlom SH, Savidge RA (2003) A reassessment of carbon content in wood: variation within and between 41 North American species. Biomass Bioenergy 25:381–388Google Scholar
  66. Lawrence DM, Thornton PE, Oleson KW, Bonan GB (2007) The partitioning of evapotranspiration into transpiration, soil evaporation, and canopy evaporation in a GCM: impacts on land atmosphere interaction. J Hydrometeorol 8:862–880Google Scholar
  67. Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol Evol 17:457–461Google Scholar
  68. Ludwig F, Jewitt RA, Donovan LA (2006) Nutrient and water addition effects on day- and night-time conductance and transpiration in a C3 desert annual. Oecologia 148:219–225PubMedGoogle Scholar
  69. Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236PubMedGoogle Scholar
  70. Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624PubMedGoogle Scholar
  71. McCormick AJ, Cramer MD, Watt DA (2006) Sink-strength regulates photosynthesis in sugarcane. New Phytol 171:759–770PubMedGoogle Scholar
  72. McCormick AJ, Cramer MD, Watt DA (2008) Changes in photosynthetic rates and gene expression of leaves during a source–sink perturbation in sugarcane. Ann Bot 101:89–102PubMedGoogle Scholar
  73. McDonald EP, Erickson JE, Kruger EL (2002) Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Funct Plant Biol 29:1115–1120Google Scholar
  74. Mengel K, Planker R, Hoffmann B (1994) Relationship between leaf apoplast pH and iron chlorosis of sunflower (Helianthus annuus L.). J Plant Nutr 17:1053–1065Google Scholar
  75. Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36Google Scholar
  76. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176PubMedGoogle Scholar
  77. Nicotra AB, Cosgrove MJ, Cowling A, Schlichting CD, Jones CS (2008) Leaf shape linked to photosynthetic rates and temperature optima in South African pelargonium species. Oecologia 154:625–635PubMedGoogle Scholar
  78. Nobel PS (1999) Physicochemical and environmental plant physiology. Academic Press, San DiegoGoogle Scholar
  79. Nye PH, Marriott FHC (1969) A theoretical study of the distribution of substances around roots resulting from simultaneous diffusion and mass-flow. Plant Soil 30:459–472Google Scholar
  80. Oaks A (1986) Biochemical aspects of nitrogen metabolism in a whole plant context. In: Lambers H, Neeteson JJ, Stulen I (eds) Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Nijhoff, Dordrecht, pp 133–151Google Scholar
  81. Onoda Y, Hirose T, Hikosaka K (2007) Effect of elevated CO2 levels on leaf starch, nitrogen and photosynthesis of plants growing at three natural CO2 springs in Japan. Ecol Res 22:475–484Google Scholar
  82. Parkhurst DF, Loucks OL (1972) Optimal leaf size in relation to environment. J Ecol 60:505–537Google Scholar
  83. Parsons LR, Kramer PJ (1974) Diurnal cycling in root resistance to water movement. Physiol Plant 30:19–23Google Scholar
  84. Patterson TB, Guy RD, Dang QL (1997) Whole-plant nitrogen- and water-relations traits, and their associated trade-offs, in adjacent muskeg and upland boreal spruce species. Oecologia 110:160–168Google Scholar
  85. Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1381–1400Google Scholar
  86. Paul M, Pellny T, Goddijn O (2001) Enhancing photosynthesis with sugar signals. Trends Plant Sci 6:197–200PubMedGoogle Scholar
  87. Pego JV, Kortsee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416PubMedGoogle Scholar
  88. Radin JW, Ackerson RC (1981) Water relations of cotton plants under nitrogen deficiency. III. Stomatal conductance, photosynthesis, and abscisic acid accumulation during drought. Plant Physiol 67:115–119PubMedGoogle Scholar
  89. Radin JW, Eidenbock MP (1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus-deficient cotton plants. Plant Physiol 75:372–377PubMedGoogle Scholar
  90. Radin JW, Parker LL (1979) Water relations of cotton plants under nitrogen deficiency. I. Dependence upon leaf structure. Plant Physiol 64:495–498PubMedGoogle Scholar
  91. Raschke K (1976) How stomata resolve the dilemma of opposing priorities. Philos Trans R Soc Lond B 273:551–560Google Scholar
  92. Raven JA, Handley LL, Wollenweber B (2004) Plant nutrition and water use efficiency. In: Bacon MS (ed) Water use efficiency in plant biology. Blackwell, OxfordGoogle Scholar
  93. Rengel Z (1993) Mechanistic simulation models of nutrient uptake: a review. Plant Soil 152:161–173Google Scholar
  94. Roessler PG, Monson RK (1985) Mid-day depression in net photosynthesis and stomatal conductance in Yucca glauca: relative contributions of leaf temperature and leaf-to-air water vapor concentration difference. Oecologia 67:380–387Google Scholar
  95. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205PubMedGoogle Scholar
  96. Roth-Nebelsick A (2001) Computer-based analysis of steady-state and transient heat transfer of small-sized leaves by free and mixed convection. Plant Cell Environ 24:631–640Google Scholar
  97. Roth-Nebelsick A (2007) Computer-based studies of diffusion through stomata of different architecture. Ann Bot 100:23–32PubMedGoogle Scholar
  98. Rufty TW Jr, Volk RJ, MacKown CT (1987) Endogenous NO3 in the root as a source of substrate for reduction in the light. Plant Physiol 84:1421–1426PubMedGoogle Scholar
  99. Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39PubMedGoogle Scholar
  100. Sankaran M, Hanan NP, Scholes RJ, Ratnam J, Augustine DJ, Cade BS, Gignoux J, Higgins SI, Le Roux X, Ludwig F, Ardo J, Banyikwa F, Bronn A, Bucini G, Caylor KK, Coughenour MB, Diouf A, Ekaya W, Feral CJ, February EC, Frost PGH, Hiernaux P, Hrabar H, Metzger KL, Prins HHT, Ringrose S, Sea W, Tews J, Worden J, Zambatis N (2005) Determinants of woody cover in African savannas. Nature 438:846–849PubMedGoogle Scholar
  101. Schäppi B, Körner CH (1997) In situ effects of elevated CO2 on the carbon and nitrogen status of alpine plants. Funct Ecol 11:290–299Google Scholar
  102. Schlesinger WH (1997) Biogeochemistry: an analysis of global change, 2nd edn. Academic Press, London, p 134Google Scholar
  103. Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Removal of nutrient limitations by long-term fertilization decreases nocturnal water loss in savanna trees. Tree Physiol 27:551–559PubMedGoogle Scholar
  104. Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038PubMedGoogle Scholar
  105. Sheen J (1994) Feedback control of gene expression. Photosynth Res 39:427–438Google Scholar
  106. Shulze E, Kelliher FM, Korner C, Lloyd J, Leuning R (1994) Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: a global ecology scaling exercise. Annu Rev Ecol Syst 25:629–662Google Scholar
  107. Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263PubMedGoogle Scholar
  108. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621Google Scholar
  109. Strebel O, Duynisveld WHM (1989) Nitrogen supply to cereals and sugar beet by mass flow and diffusion on a silty loam soil. Z Pfalnzenernãhr Bodenkd 152:135–141Google Scholar
  110. Tanner W, Beevers H (1990) Does transpiration have an essential function in long-distance ion transport in plants? Plant Cell Environ 13:745–750Google Scholar
  111. Tanner W, Beevers H (2001) Transpiration, a prerequisite for long-distance transport of minerals in plants? Proc Natl Acad Sci USA 98:9443–9447PubMedGoogle Scholar
  112. Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New YorkGoogle Scholar
  113. von Caemmerer S, Baker N (2007) The biology of transpiration: from guard cells to globe. Plant Physiol 143:3Google Scholar
  114. Wallace W (1986) Distribution of nitrate assimilation between the root and shoot of legumes and a comparison with wheat. Physiol Plant 66:630–636Google Scholar
  115. Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381Google Scholar
  116. Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487PubMedGoogle Scholar
  117. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201PubMedGoogle Scholar
  118. Wilkinson S, Corlett JE, Oger L, Davies WJ (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 117:703–709PubMedGoogle Scholar
  119. Wilkinson S, Bacon MAZ, Davies WJ (2007) Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and xylem sap pH in maize. J Exp Bot 58:1705–1716PubMedGoogle Scholar
  120. Woodward J (1699) Some thoughts and experiments concerning vegetation. Philos Trans R Soc Lond 21:193–227CrossRefGoogle Scholar
  121. Wright IJ, Reich PB, Westoby M (2003) Least-cost input mixtures of water and nitrogen for photosynthesis. Am Nat 161:98–111PubMedGoogle Scholar
  122. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827PubMedGoogle Scholar
  123. Zhang HM, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Michael D. Cramer
    • 1
    • 2
    Email author
  • Heidi-Jayne Hawkins
    • 1
  • G. Anthony Verboom
    • 1
  1. 1.Department of BotanyUniversity of Cape TownRondeboschSouth Africa
  2. 2.Faculty of Natural and Agricultural Sciences, School of Plant BiologyThe University of Western AustraliaCrawleyAustralia

Personalised recommendations