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Transcriptional Regulatory Components Responding to Macronutrient Limitation

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Abstract

The mechanisms of how plants sense nutrient availability in soils and then send the signals through downstream signal cascades are essential processes for plant survival. Although understanding the regulatory mechanisms of macronutrient sensing and signaling are very important, many components still remain unknown. This review describes the recent progress in identifying the transcriptional regulatory components that respond to phosphorus, nitrogen, potassium, and sulfur limitation. Under phosphorus limited conditions, a MYB transcription factor, PHR1, functions as a key transcriptional regulator of the phosphorus deficient responsive genes via binding to the P1BS cis element. Similarly, SLIM1 plays crucial roles in the expression of the sulfur starved responsive genes through binding to the sulfur responsive cis element. The nitrogen deficient responsive MYB transcription factors control nitrogen metabolism. Cytokinins and microRNAs (miRNAs) also mediate macronutrient metabolic processes. Much less is known about the potassium deficient signaling components, as compared to the other nutrient signaling pathways. Multiple recent studies have suggested that phytohormones, such as ethylene, auxin, jasmonic acid, and abscisic acid (ABA), and reactive oxygen species (ROS) play roles as transcriptional regulatory components in potassium deficient signaling.

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Abbreviations

bHLH:

helix–loop–helix

miRNA:

microRNA

ROS:

reactive oxygen species

References

  • Amtmann A, Hammond JP, Armengaud P, White PJ (2006) Nutrient sensing and signaling in plants: potassium and phosphorus. Adv Bot Res 43:209–257

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Armengaud P, Sulpice R, Miller AJ, Stitt M, Amtmann A, Gibon Y (2009) Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol 150:772–785

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380

    Article  PubMed  CAS  Google Scholar 

  • Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8:281

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59:2479–2497

    Article  PubMed  CAS  Google Scholar 

  • Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435

    Article  PubMed  CAS  Google Scholar 

  • Devaiah BN, Raghothama KG (2007) Transcriptional regulation of Pi starvation responses by WRKY75. Plant Signal Behav 2:424–425

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 145:147–159

    Article  PubMed  CAS  Google Scholar 

  • Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG (2009) Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2:43–58

    Article  PubMed  CAS  Google Scholar 

  • Falkenberg B, Witt I, Zanor MI, Steinhauser D, Mueller-Roeber B, Hesse H, Hoefgen R (2008) Transcription factors relevant to auxin signaling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J Exp Bot 59:2831–2846

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla JM, Martin 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

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla JM, Gonzalez 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

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla JM, Martin 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

    Article  PubMed  CAS  Google Scholar 

  • Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG (2005) Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222:730–742

    Article  PubMed  CAS  Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105:4939–4944

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132:578–596

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94:323–332

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Broadley MR, Craigon DJ, Higgins J, Emmerson ZF, Townsend HJ, White PJ, May ST (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1:10

    Article  PubMed  Google Scholar 

  • Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B, Chardakov V, Cognet-Holliger C, Colot V, Crowe M, Darimont C, Durinck S, Eickhoff H, de Longevialle AF, Farmer EE, Grant M, Kuiper MT, Lehrach H, Leon C, Leyva A, Lundeberg J, Lurin C, Moreau Y, Nietfeld W, Paz-Ares J, Reymond P, Rouze P, Sandberg G, Segura MD, Serizet C, Tabrett A, Taconnat L, Thareau V, Van Hummelen P, Vercruysse S, Vuylsteke M, Weingartner M, Weisbeek PJ, Wirta V, Wittink FR, Zabeau M, Small I (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14:2176–2189

    Article  PubMed  CAS  Google Scholar 

  • Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10205–10210

    Article  PubMed  CAS  Google Scholar 

  • Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K, Goda H, Nishizawa OI, Shibata D, Saito K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 104:6478–6483

    Article  PubMed  CAS  Google Scholar 

  • Hou XL, Wu P, Jiao FC, Jia QK, Chen HM, Yu J, Song XW, Yi KK (2005) Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signalling and hormones. Plant Cell Environ 28:353–364

    Article  CAS  Google Scholar 

  • Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607–621

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim MJ, Shin R, Schachtman DP (2009) A nuclear factor regulates abscisic acid responses in Arabidopsis. Plant Physiol 151:1433–1445

    Article  PubMed  CAS  Google Scholar 

  • Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010a) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Leigh RA, Jones RGW (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

    Article  CAS  Google Scholar 

  • Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–644

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 103:12625–12630

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (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

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004a) A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J 38:779–789

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004b) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J Exp Bot 55:1843–1849

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251

    Article  PubMed  CAS  Google Scholar 

  • Miyake K, Ito T, Senda M, Ishikawa R, Harada T, Niizeki M, Akada S (2003) Isolation of a subfamily of genes for R2R3-MYB transcription factors showing up-regulated expression under nitrogen nutrient-limited conditions. Plant Mol Biol 53:237–245

    Article  PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870

    Article  PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56:1887–1896

    Article  PubMed  CAS  Google Scholar 

  • Obertello M, Krouk G, Katari MS, Runko SJ, Coruzzi GM (2010) Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis. BMC Syst Biol 4:111

    Article  PubMed  Google Scholar 

  • O’Neill EM, Kaffman A, Jolly ER, O’Shea EK (1996) Regulation of PHO4 nuclear localization by the PHO80–PHO85 cyclin-CDK complex. Science 271:209–212

    Article  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555

    Article  PubMed  Google Scholar 

  • Peng M, Bi YM, Zhu T, Rothstein SJ (2007a) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65:775–797

    Article  PubMed  CAS  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007b) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337

    Article  PubMed  CAS  Google Scholar 

  • Peng M, Hudson D, Schofield A, Tsao R, Yang R, Gu H, Bi YM, Rothstein SJ (2008) Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. J Exp Bot 59:2933–2944

    Article  PubMed  CAS  Google Scholar 

  • Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (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

    Article  PubMed  CAS  Google Scholar 

  • Perez-Torres CA, Lopez Bucio J, Herrera Estrella L (2009) Low phosphate signaling induces changes in cell cycle gene expression by increasing auxin sensitivity in the Arabidopsis root system. Plant Signal Behav 4:781–783

    Article  PubMed  CAS  Google Scholar 

  • Rouached H, Secco D, Arpat B, Poirier Y (2011) The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol 11:19

    Article  PubMed  CAS  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martin 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

    Article  PubMed  CAS  Google Scholar 

  • Rubio V, Bustos R, Irigoyen ML, Cardona-Lopez X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69:361–373

    Article  PubMed  CAS  Google Scholar 

  • Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–195

    PubMed  CAS  Google Scholar 

  • Saito K, Hirai MY, Yonekura-Sakakibara K (2008) Decoding genes with coexpression networks and metabolomics—‘majority report by precogs’. Trends Plant Sci 13:36–43

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  PubMed  CAS  Google Scholar 

  • Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (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

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Sasakura N, Noji M, Saito K (1996) Isolation and characterization of a cDNA encoding a sulfate transporter from Arabidopsis thaliana. FEBS Lett 392:95–99

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107

    Article  PubMed  CAS  Google Scholar 

  • Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977

    Article  PubMed  CAS  Google Scholar 

  • Todd CD, Zeng P, Huete AM, Hoyos ME, Polacco JC (2004) Transcripts of MYB-like genes respond to phosphorous and nitrogen deprivation in Arabidopsis. Planta 219:1003–1009

    Article  PubMed  CAS  Google Scholar 

  • Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Garvin DF, Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Yu X, Song L, An C (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol 156:873–883

    Article  PubMed  CAS  Google Scholar 

  • Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138:2087–2096

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

This work was supported by the RIKEN President’s Discretionary Fund.

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  1. RIKEN Plant Science Center, Yokohama, Kanagawa, 230-0045, Japan

    Ryoung Shin

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Shin, R. Transcriptional Regulatory Components Responding to Macronutrient Limitation. J. Plant Biol. 54, 286–293 (2011). https://doi.org/10.1007/s12374-011-9174-7

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