Plant Molecular Biology

, 69:361 | Cite as

Plant hormones and nutrient signaling

  • Vicente Rubio
  • Regla Bustos
  • María Luisa Irigoyen
  • Ximena Cardona-López
  • Mónica Rojas-Triana
  • Javier Paz-AresEmail author


Plants count on a wide variety of metabolic, physiological, and developmental responses to adapt their growth to variations in mineral nutrient availability. To react to such variations plants have evolved complex sensing and signaling mechanisms that allow them to monitor the external and internal concentration of each of these nutrients, both in absolute terms and also relatively to the status of other nutrients. Recent evidence has shown that hormones participate in the control of these regulatory networks. Conversely, mineral nutrient conditions influence hormone biosynthesis, further supporting close interrelation between hormonal stimuli and nutritional homeostasis. In this review, we summarize these evidences and analyze possible transcriptional correlations between hormonal and nutritional responses, as a means to further characterize the role of hormones in the response of plants to limiting nutrients in soil.


Essential nutrient Plant hormone signaling Nutrient sensing Nitrogen Phosphorus Sulfur Iron Potassium Arabidopsis 



Inorganic phosphate


Pi starvation responses




Jasmonic acid


Abscisic acid






Salicylic acid


Reactive oxygen species



The authors regret that, owing to space limitations, not all relevant work on the topics described above could be cited. We thank Salomé Prat, Laurent Nussaume, and Wolf-Ruediger Scheible for critical reading of the manuscript. Research in our laboratory is supported by the Spanish Ministry of Science and Innovation (MICINN; grants BIO2005-09390 and CONSOLIDER-2007-28317; J.P.-A.) and the Comunidad de Madrid (grant S-GEN-0191-2006; V.R.). M.R.-T. and X.C.-L. are recipients of predoctoral fellowships from the Consejo Superior de Investigaciones Científicas (CSIC; JAE Program) and the Spanish MEC (FPI Program), respectively. V.R. acknowledges the support of a “Ramón y Cajal” fellowship from the Spanish MICINN.

Supplementary material

11103_2008_9380_MOESM1_ESM.xls (30 kb)
Supplementary Table 1 Data used to carry out the comparisons among transcriptional effects of nutrient starvation stresses and hormone treatments shown in Fig. 1. The upper, upper-middle and lower-middle tables, show the ratio (observed/expected), the observed number of responsive genes shared by each nutrient stress and harmonal treatment, and the expected values under random distribution, respectively. The total number of genes (“total genes”) that are up-regulated (“Up”; ≥2-fold) or down-regulated (“Down”; ≤0.5-fold) in a particular nutrient starvation stress is shown. The number of shared genes that are up- or down-regulated in response to a particular nutrient stress and hormonal treatment is indicated. The lower panel displays the chi-squared statistical significance of each observed vs. expected comparison. Transcriptiome data corresponding to CK, ABA, BR, ethylene, GA, auxin, JA and SA, and K-, N-, and S-starvation treatments was obtained from GENENVESTIGATOR (Zimmermann et al. 2004) and for the P-starvation treatment the Misson et al. (2005) data was used. (XLS 30 kb)


  1. Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576. doi: 10.1104/pp.104.046482 PubMedGoogle Scholar
  2. Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol 14:371–375PubMedGoogle Scholar
  3. Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436. doi: 10.1093/jxb/erj034 PubMedGoogle Scholar
  4. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011. doi: 10.1104/pp.106.078063 PubMedGoogle Scholar
  5. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999. doi: 10.1104/pp.106.079707 PubMedGoogle Scholar
  6. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538. doi: 10.1111/j.1365-3040.1996.tb00386.x Google Scholar
  7. Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44:314–333. doi: 10.1111/j.1365-313X.2005.02530.x PubMedGoogle Scholar
  8. Brewitz E, Larsson C-M, Larsson M (1995) Influence of nitrogen supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Physiol Plant 95:499–506. doi: 10.1111/j.1399-3054.1995.tb05515.x Google Scholar
  9. Burleigh SH, Harrison MJ (1997) A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular-arbuscular mycorrhizal (VAM) fungi and to phosphate nutrition. Plant Mol Biol 34:199–208. doi: 10.1023/A:1005841119665 PubMedGoogle Scholar
  10. Burleigh SH, Harrison MJ (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. doi: 10.1104/pp.119.1.241 PubMedGoogle Scholar
  11. Caba JM, Centeno ML, Fernández B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211:98–104Google Scholar
  12. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421. doi: 10.1105/tpc.105.038943 PubMedGoogle Scholar
  13. Ciereszko I, Kleczkowski LA (2002) Effects of phosphate deficiency and sugars on expression of rab18 in Arabidopsis: hexokinase-dependent and okadaic acid-sensitive transduction of the sugar signal. Biochim Biophys Acta 1579:43–49PubMedGoogle Scholar
  14. Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412. doi: 10.1105/tpc.104.024315 PubMedGoogle Scholar
  15. Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253. doi: 10.1016/S1369-5266(00)00168-0 PubMedGoogle Scholar
  16. Dan H, Yang G, Zheng ZL (2007) A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana. Plant Mol Biol 63:221–235. doi: 10.1007/s11103-006-9084-0 PubMedGoogle Scholar
  17. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555. doi: 10.1046/j.1365-313X.2003.01652.x PubMedGoogle Scholar
  18. Devaiah BN, Karthikeyan AS, Raghothama KG (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801. doi: 10.1104/pp.106.093971 PubMedGoogle Scholar
  19. Devaiah BN, Nagarajan VK, Raghothama KG (2007b) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 45:147–159. doi: 10.1104/pp.107.101691 Google Scholar
  20. Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a subfamily of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975. doi: 10.1111/j.1365-313X.2008.03460.x PubMedGoogle Scholar
  21. Duff SM, Moorhead GB, Lefebvre DD, Plaxton WC (1989) Phosphate starvation inducible ‘bypasses’ of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiol 90:1275–1278PubMedCrossRefGoogle Scholar
  22. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358. doi: 10.1093/jxb/erm121 PubMedGoogle Scholar
  23. Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J (2004) The transcriptional control of plant responses to phosphate limitation. J Exp Bot 55:285–293. doi: 10.1093/jxb/erh009 PubMedGoogle Scholar
  24. Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857. doi: 10.1104/pp.105.060517 PubMedGoogle Scholar
  25. Franco-Zorrilla JM, Martín AC, Solano R, Rubio V, Leyva A, Paz-Ares J (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J 32:353–360. doi: 10.1046/j.1365-313X.2002.01431.x PubMedGoogle Scholar
  26. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037. doi: 10.1038/ng2079 PubMedGoogle Scholar
  27. Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091. doi: 10.1104/pp.104.055293 PubMedGoogle Scholar
  28. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi: 10.1016/j.cub.2005.10.016 PubMedGoogle Scholar
  29. González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512. doi: 10.1105/tpc.105.036640 PubMedGoogle Scholar
  30. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. doi: 10.1016/j.pbi.2007.08.014 PubMedGoogle Scholar
  31. Haubrick LL, Assmann SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457. doi: 10.1111/j.1365-3040.2005.01481.x PubMedGoogle Scholar
  32. He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884. doi: 10.1104/pp.010843 PubMedGoogle Scholar
  33. Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617. doi: 10.1016/j.tplants.2006.10.007 PubMedGoogle Scholar
  34. Hesse H, Trachsel N, Suter M, Kopriva S, von Ballmoos P, Rennenberg H et al (2003) Effect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J Exp Bot 54:1701–1709. doi: 10.1093/jxb/erg177 PubMedGoogle Scholar
  35. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663. doi: 10.1046/j.1365-313X.2003.01658.x PubMedGoogle Scholar
  36. Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577:528–534. doi: 10.1016/j.febslet.2004.10.062 PubMedGoogle Scholar
  37. Jiang C, Fu X (2007) GA action: turning on de-DELLA repressing signaling. Curr Opin Plant Biol 10:461–465. doi: 10.1016/j.pbi.2007.08.011 PubMedGoogle Scholar
  38. Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273. doi: 10.1093/pcp/pce162 PubMedGoogle Scholar
  39. Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470. doi: 10.1104/pp.107.103788 PubMedGoogle Scholar
  40. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant miRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. doi: 10.1016/j.molcel.2004.05.027 PubMedGoogle Scholar
  41. Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hähnel U et al (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth Res 86:491–508. doi: 10.1007/s11120-005-7386-8 PubMedGoogle Scholar
  42. Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot (Lond) 97:479–495. doi: 10.1093/aob/mcl006 Google Scholar
  43. Koprivova A, Suter M, den Camp RO, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746. doi: 10.1104/pp.122.3.737 PubMedGoogle Scholar
  44. Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420. doi: 10.1104/pp.107.113175 PubMedGoogle Scholar
  45. Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T (2005) Combinatorial microarray analysis revealing arabidopsis genes implicated in cytokinin responses through the His->Asp Phosphorelay circuitry. Plant Cell Physiol 46:339–355. doi: 10.1093/pcp/pci033 PubMedGoogle Scholar
  46. Kutz A, Müller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106. doi: 10.1046/j.1365-313X.2002.01271.x PubMedGoogle Scholar
  47. Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556. doi: 10.1111/j.1365-313X.2007.03070.x PubMedGoogle Scholar
  48. Landsberg EC (1996) Hormonal regulation of iron-stress response in sunflower roots: a morphological and cytological investigation. Protoplasma 194:69–80. doi: 10.1007/BF01273169 Google Scholar
  49. Liu C, Muchhal US, Raghothama KG (1997) Differential expression of TPS11, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33:867–874. doi: 10.1023/A:1005729309569 PubMedGoogle Scholar
  50. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256. doi: 10.1104/pp.010934 PubMedGoogle Scholar
  51. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287. doi: 10.1016/S1369-5266(03)00035-9 PubMedGoogle Scholar
  52. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B et al (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691. doi: 10.1104/pp.104.049577 PubMedGoogle Scholar
  53. Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99:13938–13943. doi: 10.1073/pnas.212448699 PubMedGoogle Scholar
  54. Little YD, Rao H, Oliva S, Daniel-Vedel F, Krapp A, Malamy JE (2005) The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc Natl Acad Sci USA 102:13693–13698. doi: 10.1073/pnas.0504219102 PubMedGoogle Scholar
  55. Lucena C, Waters BM, Romera FJ, García MJ, Morales M, Alcántara E et al (2006) Ethylene could influence ferric reductase, iron transporter, and H + -ATPase gene expression by affecting FER (or FER-like) gene activity. J Exp Bot 57:4145–4154. doi: 10.1093/jxb/erl189 PubMedGoogle Scholar
  56. Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390. doi: 10.1104/pp.012161 PubMedGoogle Scholar
  57. Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd edn. Academic, LondonGoogle Scholar
  58. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605. doi: 10.1104/pp.102.019802 PubMedGoogle Scholar
  59. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J 38:779–789. doi: 10.1111/j.1365-313X.2004.02079.x PubMedGoogle Scholar
  60. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Peña A et al (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567. doi: 10.1046/j.1365-313x.2000.00893.x PubMedGoogle Scholar
  61. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R et al (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939. doi: 10.1073/pnas.0505266102 PubMedGoogle Scholar
  62. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG et al (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765. doi: 10.1073/pnas.0500778102 PubMedGoogle Scholar
  63. Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Bläsing O et al (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112. doi: 10.1111/j.1365-3040.2006.01608.x PubMedGoogle Scholar
  64. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650. doi: 10.1046/j.1365-313X.2003.01657.x PubMedGoogle Scholar
  65. Ohkama N, Goto DB, Fujiwara T, Naito S (2002) Differential tissue-specific response to sulfate and methionine of a soybean seed storage protein promoter region in transgenic Arabidopsis. Plant Cell Physiol 43:1266–1275. doi: 10.1093/pcp/pcf149 PubMedGoogle Scholar
  66. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738. doi: 10.1111/j.1365-313X.2007.03363.x PubMedGoogle Scholar
  67. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337. doi: 10.1111/j.1365-313X.2007.03050.x PubMedGoogle Scholar
  68. Philippar K, Fuchs I, Luthen H, Hoth S, Bauer CS, Haga K et al (1999) Auxin-induced K + channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci USA 96:12186–12191. doi: 10.1073/pnas.96.21.12186 PubMedGoogle Scholar
  69. Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3-induced stimulation of leaf growth. J Exp Bot 56:1143–1152. doi: 10.1093/jxb/eri107 PubMedGoogle Scholar
  70. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E et al (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211. doi: 10.1073/pnas.0605275103 PubMedGoogle Scholar
  71. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29:115–125. doi: 10.1111/j.1365-3040.2005.01405.x PubMedGoogle Scholar
  72. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A et al (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133. doi: 10.1101/gad.204401 PubMedGoogle Scholar
  73. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. doi: 10.1146/annurev.arplant.57.032905.105231 PubMedGoogle Scholar
  74. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448. doi: 10.1016/j.tplants.2006.07.004 PubMedGoogle Scholar
  75. Salama A, Wareing PF (1979) Effects of mineral nutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus L.). J Exp Bot 30:971–981. doi: 10.1093/jxb/30.5.971 Google Scholar
  76. Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69. doi: 10.1146/annurev.arplant.58.032806.103750 PubMedGoogle Scholar
  77. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N et al (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499. doi: 10.1104/pp.104.047019 PubMedGoogle Scholar
  78. Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193. doi: 10.1016/S1360-1385(03)00048-7 PubMedGoogle Scholar
  79. Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084. doi: 10.1104/pp.125.4.2078 PubMedGoogle Scholar
  80. Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118. doi: 10.1104/pp.122.4.1109 PubMedGoogle Scholar
  81. Séguéla M, Briat JF, Vert G, Curie C (2008) Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J 55:289–300. doi: 10.1111/j.1365-313X.2008.03502.x PubMedGoogle Scholar
  82. Shao HB, Chu LY, Lu ZH, Kang CM (2007) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14PubMedGoogle Scholar
  83. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832. doi: 10.1073/pnas.0401707101 PubMedGoogle Scholar
  84. Shin H, Shin HS, Chen R, Harrison MJ (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726. doi: 10.1111/j.1365-313X.2005.02629.x PubMedGoogle Scholar
  85. Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662. doi: 10.1046/j.1365-313x.2001.01185.x PubMedGoogle Scholar
  86. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A et al (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796. doi: 10.1038/ng2041 PubMedGoogle Scholar
  87. Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93. doi: 10.1093/pcp/pce009 PubMedGoogle Scholar
  88. Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K et al (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062. doi: 10.1093/pcp/pch119 PubMedGoogle Scholar
  89. Taniguchi M, Kiba T, Sakakibara H, Ueguchi C, Mizuno T, Sugiyama T (1998) Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett 429:259–262. doi: 10.1016/S0014-5793(98)00611-5 PubMedGoogle Scholar
  90. Thimm O, Blaesing O, Gibon Y, Nagel A, Meyer S, Krüger P et al (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. doi: 10.1111/j.1365-313X.2004.02016.x PubMedGoogle Scholar
  91. Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9:548–555. doi: 10.1016/j.tplants.2004.09.003 PubMedGoogle Scholar
  92. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814. doi: 10.1111/j.1365-313X.2004.02005.x PubMedGoogle Scholar
  93. Trull MC, Guiltinan MJ, Lynch JP, Deikman J (1997) The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant Cell Environ 20:85–92. doi: 10.1046/j.1365-3040.1997.d01-4.x Google Scholar
  94. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P et al (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740. doi: 10.1046/j.1365-313X.2002.01391.x PubMedGoogle Scholar
  95. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A (2004) Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J 40:523–535. doi: 10.1111/j.1365-313X.2004.02230.x PubMedGoogle Scholar
  96. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot (Lond) 97:875–881. doi: 10.1093/aob/mcj601 Google Scholar
  97. Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1, 000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567. doi: 10.1104/pp.103.021253 PubMedGoogle Scholar
  98. Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M et al (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–2522. doi: 10.1104/pp.104.044610 PubMedGoogle Scholar
  99. Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D et al (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29:1924–1935. doi: 10.1111/j.1365-3040.2006.01568.x PubMedGoogle Scholar
  100. Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA 96:15336–15341. doi: 10.1073/pnas.96.26.15336 PubMedGoogle Scholar
  101. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J et al (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397. doi: 10.1038/cr.2008.26 PubMedGoogle Scholar
  102. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409. doi: 10.1126/science.279.5349.407 PubMedGoogle Scholar
  103. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338. doi: 10.1093/jxb/erm114 PubMedGoogle Scholar
  104. Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X et al (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686. doi: 10.1104/pp.107.111443 PubMedGoogle Scholar
  105. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136(1):2621–2632. doi: 10.1104/pp.104.046367 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Vicente Rubio
    • 1
  • Regla Bustos
    • 1
  • María Luisa Irigoyen
    • 1
  • Ximena Cardona-López
    • 1
  • Mónica Rojas-Triana
    • 1
  • Javier Paz-Ares
    • 1
    Email author
  1. 1.Department of Plant Molecular GeneticsCentro Nacional de Biotecnología-CSICCantoblancoSpain

Personalised recommendations