Abstract
Sessile nature of higher plants consequently makes it highly adaptable for nutrient absorption and acquisition from soil. Plants require 17 essential elements for their growth and development which include 14 minerals (macronutrients: N, P, K, Mg, Ca, S; micronutrients: Cl, Fe, B, Mn, Zn, Cu, Ni, Mo) and 3 non-mineral (C, H, O) elements. The roots of higher plants must acquire these macronutrients and micronutrients from rhizosphere and further allocate to other plant parts for completing their life cycle. Plants evolved an intricate series of signaling and sensing cascades to maintain nutrient homeostasis and to cope with nutrient stress/availability. The specific receptors for nutrients in root, root system architecture, and internal signaling pathways help to develop plasticity in response to the nutrient starvation. Nitrogen (N), phosphorus (P), potassium (K), and sulfur (S) are essential for various metabolic processes, and their deficiency negatively effects the plant growth and yield. Genes coding for transporters and receptors for nutrients as well as some small non-coding RNAs have been implicated in nutrient uptake and signaling. This review summarizes the N, P, K, and S uptake, sensing and signaling events in nutrient stress condition especially in model plant Arabidopsis thaliana and involvement of microRNAs in nutrient deficiency. This article also provides a framework of uptake, sensing, signaling and to highlight the microRNA as an emerging major players in nutrient stress condition. Nutrient-plant-miRNA cross talk may help plant to cope up nutrient stress, and understanding their precise mechanism(s) will be necessary to develop high yielding smart crop with low nutrient input.



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Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221
Almagro A, Lin SH, Tsay YF (2008) Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell 20:3289–3299
Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52
Anjum NA, Gill R, Kaushik M, Hasanuzzaman M, Pereira E, Ahmad I, Tuteja N, Gill SS (2015) ATP-sulfurylase, sulfur-compounds and plant stress tolerance. Front Plant Sci 6:210. doi:10.3389/fpls.2015.00210
Aravind L, Koonin EV (2000) The STAS domain—a link between anion transporters and antisigma-factor antagonists. Curr Biol 10:R53–R55
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
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
Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G et al (2013) Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–373
Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13(9). doi:10.1016/j.tplants.2008.06.006
Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942
Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999
Barragan V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernandez JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142
Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorous availability. Plant Cell Environ 19:529–538
Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J, Rossignol M, Gonzalez E, Paz‐Ares J, Nussaume L (2011) Arabidopsis thaliana high‐affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23:1523–1535
Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252
Blatt MR (2004) Membrane transport in plants. Blackwell Publishing, Oxford
Bouguyon E, Gojon A, Nacry P (2012) Nitrate sensing and signaling in plants. Semin Cell Dev Biol 23:648–654
Bouguyon E, Brun F, Meynard D, Kubes M, Pervent M, Leran S, Lacombe B, Krouk G et al (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat Plants 1:15015. doi:10.1038/nplants.2015.15
Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends Plant Sci 18:325–333
Brenner WG, Romanov GA, Kollmer I, Burkle L, Schmulling 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
Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650
Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64. doi:10.1186/1471-2229-10-64
Buschmann PH, Vaidyanathan R, Gassmann W, Schroeder JI (2000) Enhancement of Na+ uptake currents, time-dependent inward-rectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiol 122:1387–1397
Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, PazAres J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102
Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530
Cakmak I, Hengeler C, Marschner H (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium-deficiency in bean-plants. J Exp Bot 45:1251–1257
Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435
Cheeseman JM, Hanson JB (1979) Mathematical analysis of the dependence of cell potential on external potassium in corn roots. Plant Physiol 63:1–4
Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P (2011) OsPHF1 regulates the plasmamembrane localization of low‐and high‐affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol 157:269–278
Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M (2003) Effects of phosphate availability on the root system architecture: large‐scale analysis of the natural variation between Arabidopsis accessions. Plant Cell Environ 26:1839–1850
Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332
Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206
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
Chiu CC, Lin CS, Hsia AP, Su RC, Lin HL, Tsay YF (2004) Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant Cell Physiol 45:1139–1148
Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Physiol 31:239–298
Clarkson DT, Diogo E, Amancio S (1999) Uptake and assimilation of sulphate by sulphur deficient Zea mays cells: the role of O-acetyl-L-serine in the interaction between nitrogen and sulphur assimilatory pathways. Plant Physiol Biochem 37:283–290
Czarnecki O, Yang J, Weston DJ, Tuskan GA, Chen J (2013) A dual role of strigolactones in phosphate acquisition and utilization in plants. Int J Mol Sci 14:7681–7701
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
David LC, Dechorgnat J, Berquin P, Routaboul JM, Debeaujon I, Daniel-Vedele F, Ferrario-Méry S (2014) Proanthocyanidin oxidation of Arabidopsis seeds is altered in mutant of the high-affinity nitrate transporter NRT2.7. J Exp Bot 65:885–893
Davidian JC, Kopriva S (2010) Regulation of sulfate uptake and assimilation: the same or not the same? Mol Plant 3:314–325
De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939–942
Dolan L (2013) Pointing PINs in the right directions: a potassium transporter is required for the polar localization of auxin efflux carriers. New Phytol 197:1027–1028
Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci U S A 49:684–692
Fang S, Yan XL, Liao H (2009) 3D reconstruction and dynamic modeling of root architecture in situ and its application to research on rice phosphorus acquisition. Plant J 60:1096–1108
Flugge U, Rainer E, Hausler RE, Ludewig F, Gierth M (2011) The role of transporters in supplying energy to plant plastids. J Exp Bot 62(7):2381–2392
Foyer CH, Noctor G, Hodges M (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62(4):1467–1482
Franco-Zorrilla JM, Martın 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
Franco-Zorrilla JM, Martın 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
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
Frank S, Tiemeyer B, Gelbrecht J, Freibauer A (2014) High soil solution carbon and nitrogen concentrations in a drained Atlantic bog are reduced to natural levels by 10 years of rewetting. Biogeosciences 11:2309–2324
Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci U S A 96:1175–1180
Fu HH, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–73
Fuchs I, Stolzle S, Ivashikina N, Hedrich R (2005) Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221:212–221
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
Gajdanowicz P, Michard E, Sandmann M, Rocha M, Correa LGG et al (2011) Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proc Natl Acad Sci U S A 108:864–869
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D et al (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655
Gierth M, Maser P (2007) Potassium transporters in plants—involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356
Gierth M, Maser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137:1105–1114
Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci U S A 105:803–808
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930
Glass ADM, Siddiqi MY (1995) Nitrogen absorption in higher plants. In: Srivastava HS, Singh RP (eds) Nitrogen nutrition in higher plants. Associated Publishing, New Delhi, pp 21–56
Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJM et al (2007) The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc Natl Acad Sci U S A 104:10726–10731
Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J Exp Bot 62:2299–2308
González-Mendoza V, Zurita-Silva A, Sánchez-Calderón L, Sánchez-Sandoval ME, Oropeza-Aburto A, Gutiérrez-Alanís D, Alatorre-Cobos F, Herrera-Estrella L (2013) APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. Plant Sci 205–206:2–12
Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605
Grennan AK (2008) Phosphate accumulation in plants: signaling. Plant Physiol 148:3–5
Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163(1):161–179
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460
Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177:889–898
Hackenberg M, Shi BJ, Gustafson P, Langridge P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13:214
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59(1):93–109
Hartje S, Zimmermann S, Klonus D, Mueller-Roeber B (2000) Functional characterisation of LKT1, a K+ uptake channel from tomato root hairs, and comparison with the closely related potato inwardly rectifying K+ channel SKT1 after expression in Xenopus oocytes. Planta 210:723–731
Hawkesford M (2003) Transporter gene families in plants: the sulphate transporter gene family–redundancy or specialization? Physiol Plant 117:155–163
He H, Liang G, Li Y, Wang F, Yu D (2014) Two young microRNAs originating from target duplication mediate nitrogen starvation adaptation via regulation of glucosinolate synthesis in Arabidopsis thaliana. Plant Physiol 164:853–865
Heber U, Viil J, Neimanis S, Mimura T, Dietz K-J (1989) Photoinhibitory damage to chloroplasts under phosphate deficiency and alleviation of deficiency and damage by photorespiratory reactions. Z Naturforsch C A J Biosci 44:524–536
Hernández I, Munne-Bosch S (2015) Linking phosphorous availability with photo-oxidative stress in plants. J Exp Bot. doi:10.1093/jxb/erv056
Hernandez M, Fernandez-Garcia N, Garcia-Garma J, Rubio-Asensio JS, Rubio F, Olmos E (2012) Potassium starvation induces oxidative stress in Solanum lycopersicum L. roots. J Plant Physiol 169:1366–1374
Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921
Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194
Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239
Hsieh LC, Lin SI, Shih ACC, Chen JW, LinW Y, Tseng CY et al (2009) Uncovering small RNA-mediated responses to phosphatedeficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132
Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156:1101–1115
Huang NC, Liu KH, Lo HJ, Tsay YF (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low affinity uptake. Plant Cell 11:1381–1392
Imamura S, Terashita M, Ohnuma M, Maruyama S, Minoda A, Weber AP, Inouye T, Sekine Y, Fujita Y, Omata T, Tanaka K (2010) Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga Cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Plant Cell Physiol 51:707–717
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Jong M, George G, Ongaro V, Williamson L, Willetts B, Ljung K, McCulloch H, Leyser O (2014) Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by N supply. Plant Physiol 166:384–395
Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021
Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-toshoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204
Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P et al (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704
Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321
Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K, Takahashi H, Dalmay T, Kopriva S (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876
Kehr J (2012) Roles of miRNAs in nutrient signaling and homeostasis. In: Sunkar R (ed) MicroRNAs in plant development and stress responses. Springer, Berlin, pp 197–217
Khan GA, Bouraine S, Wege S, Li Y, de Carbonnel M, Berthomieu P, Poirier Y, Rouached H (2014) Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis. J Exp Bot 65:871–884
Khraiwesh B, Zhu JK, Zhu JH (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148
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
Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62(4):1399–1409
Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Brehaut V, Miller A, Daniel-Vedele F, Sakakibara H et al (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24:245–258
Kim MJ, Ruzicka D, Shin R, Schachtman DP (2012) The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Mol Plant 5:1042–1057
Kirkby EA, Johnston AE (2008) Soil and fertilizer phosphorusin relation to crop nutrition. In: Hammond JP, White PJ (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 177–223
Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince A-S, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. J Exp Bot 65:789–798
Krauss G, Nies DH (2014) Ecological biochemistry: environmental and interspecies interactions, 1st edn. Wiley VCH Verlag Fmb H& Co. KGA. ISBN: 978-3-527-31650-2
Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E et al (2010a) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937
Krouk G, Mirowski P, LeCun Y, Shasha DE, Coruzzi GM (2010b) Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol 11:R123
Krouk G, Ruffel S, Gutie RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182
Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664–1672
Kuo HF, Chiou TJ (2011) The role of microRNAs in phosphorus deficiency signaling. Plant Physiol 156:1016–1024
Kutz A, Muller 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
Lacombe B, Pilot G, Michard E, Gaymard F, Sentenac H et al (2000) A Shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. Plant Cell 12:837–851
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
Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:569–593
Lapis-Gaza HR, Jost R, Finnegan PM (2014) Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol 14:334
Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot. doi:10.1093/jxb/ert474
Laugier E, Bouguyon E, Mauries A, Tillard P, Gojon A, Lejay L (2012) Regulation of high-affinity nitrate uptake in roots of Arabidopsis depends predominantly on posttranscriptional control of the NRT2.1/NAR2.1 transport system. Plant Physiol 158:1067–1078
Lebaudy A, Very AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366
Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13
Lejay L, Wirth J, Pervent M, Cross J, Tillard P, Gojon A (2008) Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol 146:2036–2053
Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165
Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci U S A 103:12625–12630
Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7(11):e48951. doi:10.1371/ journal.pone.0048951
Liang C, Wang J, Zhao J, Tian J, Liao H (2014) Control of phosphate homeostasis through gene regulation in crops. Curr Opin Plant Biol 21:59–66
Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK et al (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528
Lin WY, Lin SI, Chiou TJ (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438
Lin SI, Santi C, Jobet E, Lacut E, Kholti NE, Karlowski WM, Verdeil JL, Breitler JC, Perin C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131
Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760
Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013
Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874
Liu T, Chang C, Chiou T (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319
Liu TY, Huang TK, Tseng CY, Lai YS, Lin SI, Lin WY, Chen JW, Chiou TJ (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24:2168–2183
Liu T, Lin W, Huang T, Chiou T (2014) MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci 1–9
Lopez-Arredondo, Leyva-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:23.1–23.29
Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon 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
Lopez-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
Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-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
Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long‐distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232
Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López‐Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388
Ludewig U, von Wirén N, Rentsch D, Frommer WB (2001) Rhesus factors and ammonium: a function in efflux? Genome Biol 2:reviews 1010
Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13
Maathuis FJ (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258
Maathuis FJM, Sanders D (1994) Mechanism of high affinity potassium uptake in roots of Arabidopsis thaliana. Proc Natl Acad Sci U S A 91:9272–9276
Mahler RL (2003) General overview of nutrition for field and container crops. In: Riley LE, Dumroese RK, Landis TD Tech Coords (eds) National Proceeding: Forest and Conservation Nursery Associations. 2003 June 9-12; Coeur d Alene, ID; and 2003 July 14-17; Springfield, IL. Proc. RMRS-P-33
Marchive C, Roudier F, Castaings L, Brehaut V, Blondet E, Colot V, Meyer C, Krapp A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, San Diego
Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, De La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:1–11
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
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
Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) SLIM1/EIL3 transcription factor required for plant growth on low sulfur environment. Presented at Intl. Conf. on Arabidopsis Res., 17th, Madison, Wis
Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149
Medici A, Krouk G (2014) The primary nitrate response: a multifaceted signaling pathway. J Exp Bot 65:5567–5576
Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R, Gojon A et al (2015) AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat Commun 27(6):6274. doi:10.1038/ncomms7274
Meng YJ, Ma XX, Chen DJ, Wu P, Chen M (2010) Micro RNA mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349
Mikkelsen R, Hartz TK (2008) Nitrogen sources for organic crop production. Better Crops 92(4):16–19
Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306
Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191:149–200
Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 102:11934–11939
Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan SA, Raghothama KG et al (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A 102:7760–7765
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY et al (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012
Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arebidopsisfhaliane. Proc Natl Acad Sci U S A 9:519–523
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29
Nagarajan VK, Smith AP (2012) Ethylene’s role in phosphate starvation signaling: more than just a root growth regulator. Plant Cell Physiol 53:277–286
Nagarajan VK, Jain A, Poling MD, Lewis AJ, Raghothama KG, Smith AP (2011) Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiol 156:1149–1163
Nam YJ, Tran LSP, Kojima M, Sakakibara H, Nishiyama R et al (2012) Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS ONE 7(10):e47797. doi:10.1371/journal.pone.0047797
Natr L (1992) Mineral nutrients: a ubiquitous stress factor for photosynthesis. Photosynthetica 27:271–294
Nieves-Cordones M, Aleman F, Martinez V, Rubio F (2010) The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3:326–333
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
Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318
Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2012) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408
Nunes CM, O’Hara L, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013) The trehalose 6-phosphate/SnRK1 signalling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732
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
Orsel M, Filleur S, Fraisier V, Daniel-Vedele F (2002) Nitrate transport in plants: which gene and which control? J Exp Bot 53:825–833
Ostaszewska M, Juszczuk IM, Kołodziejek I, Rychter AM (2014) Long-term sulphur starvation of Arabidopsis thaliana modifies mitochondrial ultrastructure and activity and changes tissue energy and redox status. J Plant Physiol 171(7):549–558
Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845
Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J et al (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNAsequencing. Plant Physiol 150:1541–1555
Pao SS, Paulsen IT, Saier MH (1996) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 68(507). doi:10.1038/nature13116
Perez-Torres CA, Lopez-Bucio J, Cruz-Ramırez A et al (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272
Philippar K, Fuchs I, Luthen H, Hoth S, Bauer CS, Haga K, Thiel G, Ljung K, Sandberg G, Bottger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci U S A 96:12186–12191
Puga MI, Mateos I, Charukesi R, Wang Z, Franco-Zorrilla JM, Lorenzoa L, Irigoyen ML, Masierod S, Bustos R, Rodríguez J, Leyva A, Rubio V, Sommer H, Paz-Ares J (2014) SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc Natl Acad Sci U S A 111(41):14947–14952
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693
Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49
Ramaiah M, Jain A, Raghothama KG (2014) ETHYLENE RESPONSE FACTOR070 regulates root development and phosphate starvation-mediated responses. Plant Physiol 164:1484–1498
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37
Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509
Ren XL, Qi GN, Feng HQ, Zhao S, Zhao SS et al (2013) Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J 74:258–266
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
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Venek EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156
Rigas S, Debrosses G, Haralampidis K et al (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13:139–151
Rigas S, Ditengou FA, Ljung K et al (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141
Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133
Rubio V, Bustos R, Irigoyen ML, Cardona-López X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69:361–373
Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci U S A 108:18524–18529
Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450
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
Salsac L, Chaillou S, Morot-Gaudry JF, Lesaint C, Jolivet E (1987) Nitrate and ammonium nutrition in plants. Plant Physiol Biochem 25:805–812
Sanchez-Calderon L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184
Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453
Scheible WR, Pant B, Musialak-Lange M, Nuc P (2011) Nutrient-responsive plant microRNAs. In: Erdmann VA, Barciszewski J (eds) Non coding RNAs in plants. Springer, Berlin, pp 313–337
Schroeder JI, Fang HH (1991) Inward-rectifying K+ channels in guard cells provides a mechanism for low-affinity K+ uptake. Proc Natl Acad Sci U S A 88:11583–11587
Schroeder JI, Ward JM, Gassmann W (1994) Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu Rev Biophys Biomol Struct 23:441–471
Secco D, Jabnoune M, Walker H, Shou H, Wu P, Poirier Y, Whelan J (2013) Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell 25:4285–4304
Segonzac C, Boyer JC, Ipotesi E, Szponarski W, Tillard P, Touraine B, Sommerer N, Rossignol M, Gibrat R (2007) Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell 19:3760–3777
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005
Shen C, Wang S et al (2013) OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryzasativa L.). Plant Cell Environ 36:607–620
Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642
Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357
Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc B 367:1441–1452
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149
Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, van den Berg PJ, Belcher AR, Warrilow AGS (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 12:875–884
Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR et al (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity. J Gen Physiol 113:909–918
Stacey MG, Osawa H, Patel A, Gassmann W, Stacey G (2006) Expression analyses of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta 223:291–305
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L et al (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182
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
Tang Z, Fan X, Li Q, Feng H, Miller AJ, Shen Q, Xu G (2012) Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root in flux. Plant Physiol 160:2052–2063
Thibaud MC, Arrighi J-F, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789
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
Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6(7):e1001031. doi:10.1371/journal.pgen.1001031
Tsay YF et al (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713
Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:1751–1766
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
Victoria J, Nikiforova VJ, Kopka J et al (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plant. Plant Physiol 138:304–318
Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutierrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:4477–4482
Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci U S A 110:12840–12845
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687
von der Fecht-Bartenbach J et al (2010) CLC-b-mediated NO3 -/H+ exchange across the tonoplast of Arabidopsis vacuoles. Plant Cell Physiol 51(960–968):43
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
Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proc Natl Acad Sci U S A 93:10510–10514
Wang YY, Tsay YF (2011) Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–1957
Wang Y, Wu W (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451–476
Wang R et al (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci U S A 95:15134–15139
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
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
Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29:1924–1935
Wang C, Huang W, Ying Y, Li S, Secco D, Tyerman S, Whelan J, Shou H (2012a) Functional characterization of the rice SPXMFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves. New Phytol 196:139–148
Wang Y, Hsu P, Tsay Y (2012b) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8):458–467
Wang J, Sun J, Miao J, Guo J, Shi Z, He M, Chen Y, Zhao X, Li B, Han F et al (2013) A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann Bot 111:1139–1153
Wang Z, Ruan W, Shi J, Zhang L, Xiang D, Yang C, Li C, Wu Z, Liu Y, Yu Y, Shou H, Mo X, Mao C, Wu P (2014) Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci U S A 111(41):14953–14958
Waraich EA, Ahmad R, Saifullah, Ashraf MY, Ehsanullah (2011) Role of mineral nutrition in alleviation of drought stress in plants. Aust J Crop Sci 5:764–777
Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882
Wu G (2013) Plant microRNAs and development. J Genet Genomics 40:217–230
Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16:205–212
Xu J, Li HD, Chen LQ, Wang Y, Liu LL et al (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360
Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J et al (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14:66
Yi H, Galant A, Ravilious GE, Preuss ML, Jez JM (2010) Sensing sulfur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol Plant 3:269–279
Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates redistribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131:1511–1517
Yuan L, Loque D, Kojima S, Rauch S, Ishiyama K et al (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652
Zeng H, Wang G, Hu X, Wang H, Du L, Zhu Y (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374:1005–1021
Zhang Z, Liao H, Lucas WJ (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56:192–220
Zhao DL, Oosterhuis DM, Bednarz CW (2001) Influences of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosyntetica 39:103–199
Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915
Zimmermann S, Talke I, Ehrhardt T, Nast G, Muller-Rober B (1998) Characterization of SKT1, an inwardly rectifying potassium channel from potato, by heterologous expression in insect cells. Plant Physiol 116:879–890
Acknowledgments
NT is thankful to Indo–French Centre for the Promotion of Advanced Research (IFCPAR/CEFIPRA) for financial support of this work (Proposal No. 4609-A). We are also thankful to Drs. Gabrial Krouk (BPMP, Montpellier Cedex, France) and Ananda K. Sarkar (NIPGR, New Delhi) for their critical reading of the manuscript.
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Nath, M., Tuteja, N. NPKS uptake, sensing, and signaling and miRNAs in plant nutrient stress. Protoplasma 253, 767–786 (2016). https://doi.org/10.1007/s00709-015-0845-y
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DOI: https://doi.org/10.1007/s00709-015-0845-y