Plant and Soil

, Volume 232, Issue 1–2, pp 51–68 | Cite as

The nutritional control of root development

  • Brian Forde
  • Helena Lorenzo
Article

Abstract

Root development is remarkably sensitive to variations in the supply and distribution of inorganic nutrients in the soil. Here we review examples of the ways in which nutrients such as N, P, K and Fe can affect developmental processes such as root branching, root hair production, root diameter, root growth angle, nodulation and proteoid root formation. The nutrient supply can affect root development either directly, as a result of changes in the external concentration of the nutrient, or indirectly through changes in the internal nutrient status of the plant. The direct pathway results in developmental responses that are localized to the part of the root exposed to the nutrient supply; the indirect pathway produces systemic responses and seems to depend on long-distance signals arising in the shoot. We propose the term `trophomorphogenesis' to describe the changes in plant morphology that arise from variations in the availability or distribution of nutrients in the environment. We discuss what is currently known about the mechanisms of external and internal nutrient sensing, the possible nature of the long-distance signals and the role of hormones in the trophomorphogenic response.

Nitrate nutrients plasticity root development signalling trophomorphogenesis 

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References

  1. Ballaré C L 1999 Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci. 4, 97–102.Google Scholar
  2. Bariola P A, Howard C J, Taylor C B, Verburg M T, Jaglan V D and Green P J 1994 The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 6, 673–685.Google Scholar
  3. Bates T R and Lynch J P 1996 Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ. 19, 529–538.Google Scholar
  4. Bazzaz F A, Garbutt K, Reekie E G and Williams W E 1989 Using growth analysis to interpret competition between a C3 and a C4 annual under ambient and elevated CO2. Oecologia 79, 223–225.Google Scholar
  5. Bhat K K S, Nye P H and Bereton A J 1979 The possibility of predicting solute uptake and plant growth responses from independently measured soil and plant characteristics. VI. The growth and uptake of rape in solutions of constant nitrate concentration. Plant Soil 53, 137–167.Google Scholar
  6. Bienfait H F 1988 Proteins under the control of the gene for Fe efficiency in tomato.Plant Physiol. 88, 785–787.Google Scholar
  7. Bilbrough C J and Caldwell M M 1995 The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field. Oecologia 103, 10–16.Google Scholar
  8. Bonser A M, Lynch J and Snapp S 1996 Effect of phosphorus de-ficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol. 132, 281–288.Google Scholar
  9. Boot R G A and Mensink M 1990 Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant Soil 129, 291–299.Google Scholar
  10. Burleigh S H and Harrison M J 1999 The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol. 119, 241–248.Google Scholar
  11. Cahn M D, Zobel RWand Bouldin D R 1989 Relationship between root elongation rate and diameter and duration of growth of lateral roots of maize. Plant Soil 119, 271–279.Google Scholar
  12. Carroll B J and Gresshoff P M 1983 Nitrate inhibition of nodulation and nitrogen-fixation in white clover. Z. Pflanzenphysiol. 110, 77–88.Google Scholar
  13. Carroll B J and Gresshoff P M 1986 Isolation and initial characterization of constitutive nitrate reductase-deficient mutants nr328 and nr345 of soybean (Glycine max). Plant Physiol. 81, 572–576.Google Scholar
  14. Carroll B J and Mathews A 1990 Nitrate inhibition of nodulation in legumes. In Molecular Biology of Symbiotic Nitrogen Fixation. Ed. P M Gresshoff. pp 159–180. CRC Press, Boca Raton, FL.Google Scholar
  15. Carroll B J, McNeil D L and Gresshoff PM1985 Isolation and properties of soybean [Glycine max (L.) Merr] mutants that nodulate in the presence of high nitrate concentrations. Proc. Natl. Acad. Sci. USA. 82, 4162–4166.Google Scholar
  16. Carswell M C, Grant B R and Plaxton W C 1997 Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide phosphonate. Planta 203, 67–74.Google Scholar
  17. Chapin F S I 1980 The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233–260.Google Scholar
  18. Citovsky V and Zambryski P 2000 Systemic transport of RNA in plants. Trends Plant Sci. 5, 52–54.Google Scholar
  19. Coleman J S, McConnaughay K D M and Ackerly D D 1994 Interpreting developmental variation in plants. Trends Ecol. Evol. 9, 187–191.Google Scholar
  20. Cooper H D and Clarkson D T 1989 Cycling of amino nitrogen and other nutrients between shoots and roots in cereals: a pos-sible mechanism integrating shoot and root in the regulation of nutrient uptake. J. Exp. Bot. 40, 753–762.Google Scholar
  21. Couot-Gastelier J and Vartanian N 1995 Drought-induced short roots in Arabidopsis thaliana: structural characteristics. Bot. Acta 108, 407–413.Google Scholar
  22. Day D A, Lambers H, Bateman J, Carroll B J and Gresshoff P M 1986 Growth comparisons of a supernodulating soybean (Glycine max) mutant and its wild-type parent. Physiol. Plant. 68, 375–382.Google Scholar
  23. Day D A, Carroll B J, Delves A C and Gresshoff PM 1989 Relationship between auto-regulation and nitrate inhibition of nodulation in soybeans. Physiol. Plant. 75, 37–42.Google Scholar
  24. Delves A C, Higgins A V and Gresshoff P M 1987 Shoot control of supernodulation in a number of mutant soybeans, Glycine max (L.) Merr. Aust. J. Plant Physiol. 14, 689–694.Google Scholar
  25. Deng M D, Moureaux T and Caboche M 1989 Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol. 91, 304–309.Google Scholar
  26. Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183–200.Google Scholar
  27. Drew M C 1975 Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75, 479–490.Google Scholar
  28. Drew M C and Saker L R 1975 Nutrient supply and the growth of the seminal root system of barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J. Exp. Bot. 26, 79–90.Google Scholar
  29. Drew M C and Saker L R 1978 Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake in response to a localized supply of phosphate. J. Exp. Bot. 29, 435–451.Google Scholar
  30. Drew M C, Saker L R and Ashley T W 1973 Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. J. Exp. Bot. 24, 1189–1202.Google Scholar
  31. Ericsson T 1995 Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169, 205–214.Google Scholar
  32. Evans G C 1972 The Quantitative Analysis of Plant Growth. University of California Press.Google Scholar
  33. Ferris P J and Goodenough U W 1997 Mating type in Chlamydomonas is specified by Mid, the minus dominance gene. Genetics 146, 859–869.Google Scholar
  34. Fitter A H 1976 Effects of nutrient supply and competition from other species on root growth of Lolium perenne in soil. Plant Soil 45, 177–189.Google Scholar
  35. Fitter A H 1985 Functional significance of root morphology and root system architecture. In Ecological Interactions in Soil, Special Publication of the British Ecological Society, No. 4. Ed. A H Fitter, D Atkinson, D J Read, and M B Usher. pp 87–106. Blackwell Scientific, Oxford.Google Scholar
  36. Fitter A H 1987 An architectural approach to the comparative ecology of plant-root systems. New Phytol. 106 (Suppl), 61–77.Google Scholar
  37. Foehse D and Jungk A 1983 Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74, 359–368.Google Scholar
  38. Forde B G and Clarkson D T 1999 Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv. Bot. Res. 30, 1–90.Google Scholar
  39. Francisco P B and Akao S 1993 Autoregulation and nitrate inhibition of nodule formation in soybean cv Enrei and its nodulation mutants. J. Exp. Bot. 44, 547–553.Google Scholar
  40. Friend A L, Eide M R and Hinckley TM 1990 Nitrogen stress alters root proliferation in Douglas fir seedlings. Can. J. For. Res. 20, 1524–1529.Google Scholar
  41. Furuya M and Kim B C 2000 Do phytochromes interact with diverse partners? Trends Plant Sci. 5, 87–89.Google Scholar
  42. Gahoonia T S and Nielsen N E 1997 Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.Google Scholar
  43. Ge Z Y, Rubio G and Lynch J P 2000 The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218, 159–171.Google Scholar
  44. Genoud T and Métraux J-P 1999 Crosstalk in plant cell signaling: structure and function of the genetic network. Trends Plant Sci. 4, 503–507.Google Scholar
  45. Gilbert G A, Knight J D, Vance C P and Allan D L 2000 Proteoid root development of phosphorous deficient lupin is mimicked by auxin and phosphonate. Ann. Bot. 85, 921–928.Google Scholar
  46. Gilroy S and Jones D L 2000 Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 5, 56–60.Google Scholar
  47. Gresshoff P M, Krotzky A, Mathews A, Day D A, Schuller K A, Olsson J, Delves A C and Carroll B J 1988 Suppression of the symbiotic supernodulation symptoms of soybean. J. Plant Physiol. 132, 417–423.Google Scholar
  48. Grime J P, Crick J C and Rincon J E 1986 The ecological significance of plasticity. In Plasticity in Plants. Ed. D H Jennings and A J Trewavas. pp 5–29. Biologists Limited, Cambridge.Google Scholar
  49. Grusak M A and Pezeshgi S 1996 Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol. 110, 329–334.Google Scholar
  50. Hackett C 1967 A study of the root system of barley. I. Effects of nutrition on two varieties. New Phytol. 67, 287–289.Google Scholar
  51. Hackett C 1972 A method of applying nutrients locally to roots under controlled conditions, and some morphological effects of locally applied nitrate on the branching of wheat roots. Aust. J. Biol. Sci. 25, 1169–1180.Google Scholar
  52. Heard J, Caspi M and Dunn K 1997 Evolutionary diversity of symbiotically induced nodule MADS box genes: characterization of nmhC5, a member of a novel subfamily. Mol. Plant-Microbe Interact. 10, 665–676.Google Scholar
  53. Heidstra R, Geurts R, Franssen H, Spaink H P, van Kammen A and Bisseling T 1994 Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105, 787–797.Google Scholar
  54. Heidstra R, Nilsen G, Martinez Abarca F, van Kammen A and Bisseling T 1997 Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Mol. Plant-Microbe Interact. 10, 215–220.Google Scholar
  55. Hinson K 1975 Nodulation responses from nitrogen applied to soybean half-root systems. Agron. J. 67, 799–804.Google Scholar
  56. Hobbie L and Estelle M 1995 The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J. 7, 211–220.Google Scholar
  57. Hodge A, Robinson D, Griffiths B S and Fitter A H 1999 Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete Plant Cell Environ. 22, 811–820.Google Scholar
  58. Hsieh M-H, Lam H-M, Van De Loo F J and Coruzzi G 1998 A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc. Natl Acad Sci USA 95, 13965–13970.Google Scholar
  59. Hunter W J 1993 Ethylene production by root nodules and effect of ethylene on nodulation in Glycine max. Appl. Environ. Microbiol. 59, 1947–1950.Google Scholar
  60. Hutchings M J and de Kroon H 1994 Foraging in plants: the role of morphological plasticity in resource acquisition. Adv. Ecol. Res. 25, 159–238.Google Scholar
  61. Imsande J and Touraine B 1994 N demand and the regulation of nitrate uptake. Plant Physiol. 105, 3–7.Google Scholar
  62. Jacobsen E 1984 Modification of symbiotic interaction of pea (Pisum sativum L.) and Rhizobium leguminosarum by induced mutations. Plant Soil 82, 427–438.Google Scholar
  63. Johnson J F, Allan D L and Vance C P 1994 Phosphorus stressinduced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol. 104, 657–665.Google Scholar
  64. Keerthisinghe G, Hocking P J, Ryan P R and Delhaize E 1998 Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ. 21, 467–478.Google Scholar
  65. Klasson H, Fink G R and Ljungdahl P O 1999 Ssy1p and Ptr3p are plasma membrane components of a yeast system that senses extracellular amino acids. Mol. Cell. Biol. 19, 5405–5416.Google Scholar
  66. Kohls S J and Baker D D 1989 Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants. Plant Soil 118, 171–179.Google Scholar
  67. Kosslak R M and Bohlool B B 1984 Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol. 75, 125–130.Google Scholar
  68. Lainé P, Ourry A and Boucaud J 1995 Shoot control of nitrate uptake rates by roots of Brassica napus L. Effects of localized nitrate supply. Planta 196, 77–83.Google Scholar
  69. Lee K H and La Rue T A 1992 Ethylene as a possible mediator of light-induced and nitrate-induced inhibition of nodulation of Pisum sativum L. cv Sparkle. Plant Physiol. 100, 1334–1338.Google Scholar
  70. Liao H and Yan X L 2000 Adaptive changes and genotypic variation for root architecture of common bean in response to phosphorus deficiency. Acta Bot. Sin. 42, 158–163.Google Scholar
  71. Ligero F, Caba J M, Lluch C and Olivares J 1991 Nitrate inhibition of nodulation can be overcome by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol. 97, 1221–1225.Google Scholar
  72. Ligero F, Poveda J L, Gresshoff PM and Caba JM1999 Nitrate-and inoculation-enhanced ethylene biosynthesis in soybean roots as a possible mediator of nodulation control. J. Plant Physiol. 154, 482–488.Google Scholar
  73. Ling H Q, Pich A, Scholz G and Ganal M W 1996 Genetic analysis of two tomato mutants affected in the regulation of iron metabolism. Mol. Gen. Genet. 252, 87–92.Google Scholar
  74. Lorenz M C and Heitman J 1998 The MEP2 ammonium permease regulates pseudohyphal differentiaition in Saccharomyces cerevisiae. EMBO J. 17, 1236–1247.Google Scholar
  75. Lucas W J 1997 Application of microinjection techniques to plant nutrition. Plant Soil 196, 175–189.Google Scholar
  76. Lynch J and Brown K M 1997 Ethylene and plant responses to nutritional stress. Physiol. Plant. 100, 613–619.Google Scholar
  77. Malik N S A, Calvert H E and Bauer W D 1987 Nitrate-induced regulation of nodule formation in soybean. Plant Physiol. 84, 266–271.Google Scholar
  78. Marschner H 1995 Mineral Nutrition of Higher Plants. Academic Press, London. Melcior W and Steudle E 1993 Water transport in onion (Allium cepa L.) roots: changes of axial and radial hydraulic conductivities during root development. Plant Physiol. 101, 1305–1315.Google Scholar
  79. Merrick M J and Edwards R A 1995 Nitrogen control in bacteria. Microbiol. Rev. 59, 604–622.Google Scholar
  80. Mollier A and Pellerin S 1999 Maize root system growth and development as influenced by phosphorus deficiency. J. Exp. Bot. 50, 487–497.Google Scholar
  81. Moog P R, Vanderkooij T A W, Bruggemann W, Schiefelbein J W and Kuiper P J C 1995 Responses to iron deficiency in Arabidopsis thaliana: the turbo iron reductase does not depend on the formation of root hairs and transfer cells. Planta 195, 505–513.Google Scholar
  82. Nobbe F 1862 Uber die feinere Verästelung der Pflanzenwurzeln. Landwirtschaft. VersStat. 4, 212–224.Google Scholar
  83. Ozcan S, Dover J, Rosenwald A G, Wolfl S and Johnston M 1996 Two glucose transporters in Saccharomyces cerevisiae are glucose sensors that generate a signal for induction of gene expression. Proc. Natl. Acad. Sci. USA 93, 12428–12432.Google Scholar
  84. Peuke A D, Hartung W and Jeschke WD 1994 The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. II. Grown with low or high nitrate supply. J. Exp. Bot. 45, 733–740.Google Scholar
  85. Postma J G, Jacobsen E and Feenstra W J 1988 Three pea mutants with an altered nodulation studied by genetic analysis and grafting. J. Plant Physiol. 132, 424–430.Google Scholar
  86. Pouteau S, Cherel I, Vaucheret H and Caboche M 1989 Nitrate reductase mRNA regulation in Nicotiana plumbaginifolia nitrate reductase-deficient mutants. Plant Cell 1, 1111–1120.Google Scholar
  87. Pozuelo M, Merchán F, Macías M I, Beck CF, Galván A, Fernández E 2000 The negative effect of nitrate on gametogenesis is independent of nitrate assimilation in Chlamydomonas reinhardti Planta 211, 287–292.Google Scholar
  88. Robinson D 1994 The responses of plants to non-uniform supplies of nutrients. New Phytol. 127, 635–674.Google Scholar
  89. Robinson D and Rorison I H 1983 A comparison of the responses of Lolium perenne L., Holcus lanatus L. and Deschampsia flexuosa (L.) Trin. to a localized supply of nitrogen. New Phytol. 94, 263–273.Google Scholar
  90. Robinson D and Rorison I H 1987 Root hairs and plant growth at low nitrogen availabilities.New Phytol. 107, 681–693.Google Scholar
  91. Robinson D, Hodge A, Griffiths B S and Fitter A H 1999 Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc. R. Soc. Londen Ser. B 26, 431–435.Google Scholar
  92. Ruiz-Medrano R, Xoconostle-Cazares B and Lucas W J 1999 Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405–4419.Google Scholar
  93. Ryan C A 2000 The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477, 112–121.Google Scholar
  94. Ryser P, Verduyn B and Lambers H 1997 Phosphorus allocation and utilization in three grass species with contrasting response to N and P supply. New Phytol. 137, 293–302.Google Scholar
  95. Sattelmacher B and Thoms K 1995 Morphology and physiology of the seminal root system of young maize (Zea mays L.) plants as influenced by a locally restricted nitrate supply. Z. Pflanzen. Bodenk. 158, 493–497.Google Scholar
  96. Schauser L, Roussis A, Stiller J and Stougaard J 1999 A plant regulator controlling development of symbiotic root nodules. Nature 402, 191–195.Google Scholar
  97. Scheible W R, Gonzalez-Fontes A, Lauerer M, Müller-Röber B, Caboche M and Stitt M 1997a Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9, 783–798.Google Scholar
  98. Scheible W R, Lauerer M, Schulze E D, Caboche M and Stitt M 1997b Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J. 11, 671–691.Google Scholar
  99. Schiefelbein J, Galway M, Masucci J and Ford S 1993 Pollen tube and root hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol. 103, 979–985.Google Scholar
  100. Schmidt J S, Harper J E, Hoffman T K and Bent A F 1999 Regulation of soybean nodulation independent of ethylene signaling. Plant Physiol. 119, 951–959.Google Scholar
  101. Schmidt W 1999 Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol. 141, 1–26.Google Scholar
  102. Schmidt W, Tittel J and Schikora A 2000 Role of hormones in the induction of iron deficiency responses in Arabidopsis roots.Plant Physiol. 122, 1109–1118.Google Scholar
  103. Scholz G, Becker R, Pich A and Stephan U W 1992 Nicotianamine: a common constituent of strategy I and strategy II of iron acquisition by plants – a review. J. Plant Nutr. 15, 1647–1665.Google Scholar
  104. Schultze M and Kondorosi A 1998 Regulation of symbiotic root nodule development. Ann. Rev. Genet. 32, 33–57.Google Scholar
  105. Shore P and Sharrocks A D 1995 The MADS-box family of transcription factors. Eur. J. Biochem. 229, 1–13.Google Scholar
  106. Skene K R 2000 Cluster roots: their physiology, ecology and developmental biology. Ann. Bot. 85, 899–899.Google Scholar
  107. Snapp S, Koide R and Lynch J 1995 Exploitation of localized phosphorus-patches by common bean roots. Plant Soil 177, 211–218.Google Scholar
  108. Stitt M and Feil R 1999 Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root. Plant Soil 215, 143–153.Google Scholar
  109. Thaler P and Pages L 1996 Root apical diameter and root elongation rate of rubber seedlings (Hevea brasiliensis) show parallel responses to photoassimilate availability. Physiol. Plant. 97, 365–371.Google Scholar
  110. Thompson G A and Schulz A 1999 Macromolecular trafficking in the phloem. Trends Plant Sci. 4, 354–360.Google Scholar
  111. Thornton H G 1936 The action of sodium nitrate upon the infection of lucerne root-hairs by nodule bacteria. Proc. R. Soc. London Ser. B 119, 474–491.Google Scholar
  112. Tillard P, Passama L and Gojon A 1998 Are phloem amino acids involved in the shoot to root control of NO3 uptake in Ricinus communis plants? J. Exp. Bot. 49, 1371–1379.Google Scholar
  113. Trull M C, Guiltinan M J, Lynch J P and Deikman J 1997 The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant Cell Environ. 20, 85–92.Google Scholar
  114. von Arnim A G 1999 Phytochrome in the limelight. Trends Plant Sci. 4, 465–466.Google Scholar
  115. Watt M and Evans J R 1999 Proteoid roots. Physiology and development. Plant Physiol. 121, 317–323.Google Scholar
  116. Whiting S N, Leake J R, McGrath S P and Baker A J M 2000 Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol. 145, 199–210.Google Scholar
  117. Wiersum L K 1958 Density of root branching as affected by substrate and separate ions. Acta Bot. Neerl. 7, 174–190.Google Scholar
  118. Wilson J K 1917 Physiological studies of Bacillus radicicola or soybean (Soja max Piper) and factors influencing nodule production. Cornell Univ. Agric. Exp. Stn. Bull. 386, 369.Google Scholar
  119. Zhang H and Forde B G 1998 An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.Google Scholar
  120. Zhang H, Jennings A J, Barlow P W and Forde B G 1999 Dual pathways for regulation of root branching by nitrate. Proc. Natl Acad. Sci. USA 96, 6529–6534.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Brian Forde
    • 1
  • Helena Lorenzo
    • 2
  1. 1.Department of Biological SciencesLancaster UniversityLancasterUK
  2. 2.Biochemistry and Physiology DepartmentIACR-RothamstedHarpendenUK

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