Abstract
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.
Similar content being viewed by others
Abbreviations
- Pi:
-
Inorganic phosphate
- PSR:
-
Pi starvation responses
- CK:
-
Cytokinins
- JA:
-
Jasmonic acid
- ABA:
-
Abscisic acid
- GA:
-
Gibberellins
- BR:
-
Brassinosteroids
- SA:
-
Salicylic acid
- ROS:
-
Reactive oxygen species
References
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
Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol 14:371–375
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
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
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
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
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
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
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
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
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 211:98–104
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
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 1579:43–49
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
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
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
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
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
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
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
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 90:1275–1278
Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358. doi:10.1093/jxb/erm121
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
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
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
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
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
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
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
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. doi:10.1016/j.pbi.2007.08.014
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
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
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
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
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
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
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
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
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
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
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
Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot (Lond) 97:479–495. doi:10.1093/aob/mcl006
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd edn. Academic, London
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. doi:10.1146/annurev.arplant.57.032905.105231
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
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
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
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
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
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
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
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
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 4:8–14
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
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)
Rights and permissions
About this article
Cite this article
Rubio, V., Bustos, R., Irigoyen, M.L. et al. Plant hormones and nutrient signaling. Plant Mol Biol 69, 361–373 (2009). https://doi.org/10.1007/s11103-008-9380-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-008-9380-y