Skip to main content

Advertisement

SpringerLink
Log in

Role of microRNAs in plant responses to nutrient stress

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background

Plants must acquire at least 14 mineral nutrients from the soil to complete their life cycles. Insufficient availability or extreme high levels of the nutrients significantly affect plant growth and development. Plants have evolved a series of mechanisms to adapt to unsuitable growth conditions where nutrient levels are too low or too high. microRNAs (miRNAs), a class of small RNAs, are known to mediate post-transcriptional regulation by transcript cleavage or translational inhibition. Besides regulating plant growth and development, miRNAs are well documented to regulate plant adaptation to adverse environmental conditions including nutrient stresses.

Scope

In this review, we focus on recent progress in our understanding of how miRNAs are involved in plant response to stresses resulting from deficiency in nutrients, such as nitrogen, phosphorus, sulfur, copper and iron, as well as toxicities from heavy metal ions.

Conclusions

Accumulated evidence indicates that miRNAs play critical roles in sensing the abundance of nutrients, controlling nutrient uptake and phloem-mediated long-distance transport, and nutrient homeostasis. miRNAs act as systemic signals to coordinate these physiological activities helping plants respond to and survive nutrient stresses and toxicities. Knowledge about how miRNAs are involved in plant responses to nutrient stresses promise to provide novel strategies to develop crops with improved nutrient use efficiency which could be grown in soils with either excessive or insufficient availability of nutrients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    CAS  PubMed  Google Scholar 

  • Alam SM (1999) Nutrient uptake by plants under stress conditions. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press, Marcel Dekker Inc, New York, pp 285–313

    Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G, Park J, Shen M, Hong H, Kim WY, Kim DH, Lee SY, Bressan RA, Bohnert HJ, Yun DJ (2013) Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–373

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beauclair L, Yu A, Bouche N (2010) microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62:454–462

    CAS  PubMed  Google Scholar 

  • Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant Microbe Interact 23:915–926

    CAS  PubMed  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    CAS  PubMed  Google Scholar 

  • Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749

    CAS  PubMed  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    PubMed Central  PubMed  Google Scholar 

  • Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    CAS  PubMed  Google Scholar 

  • Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Perez-Perez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102

    PubMed Central  PubMed  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    CAS  PubMed  Google Scholar 

  • Chen ZH, Bao ML, Sun YZ, Yang YJ, Xu XH, Wang JH, Han N, Bian HW, Zhu MY (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 77:619–629

    CAS  PubMed  Google Scholar 

  • Chen L, Wang T, Zhao M, Tian Q, Zhang WH (2012) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235:375–386

    CAS  PubMed  Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    CAS  PubMed  Google Scholar 

  • Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Physiol 31:239–298

    CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    CAS  PubMed  Google Scholar 

  • Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088

    CAS  PubMed  Google Scholar 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573

    CAS  PubMed  Google Scholar 

  • Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138:778–789

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417

    CAS  PubMed  Google Scholar 

  • Fischer JJ, Beatty PH, Good AG, Muench DG (2013) Manipulation of microRNA expression to improve nitrogen use efficiency. Plant Sci 210:70–81

    CAS  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Gao N, Su Y, Min J, Shen W, Shi W (2010) Transgenic tomato overexpressing ath-miR399d has enhanced phosphorus accumulation through increased acid phosphatase and proton secretion as well as phosphate transporters. Plant Soil 334:123–136

    CAS  Google Scholar 

  • Gielen H, Remans T, Vangronsveld J, Cuypers A (2012) MicroRNAs in metal stress: specific roles or secondary responses? Int J Mol Sci 13:15826–15847

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Google Scholar 

  • Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237

    CAS  PubMed  Google Scholar 

  • Hackenberg M, Huang PJ, Huang CY, Shi BJ, Gustafson P, Langridge P (2013) A comprehensive expression profile of microRNAs and other classes of non-coding small RNAs in barley under phosphorous-deficient and -sufficient conditions. DNA Res 20:109–125

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hell R, Stephan U (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551

    CAS  PubMed  Google Scholar 

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang SQ, Peng J, Qiu CX, Yang ZM (2009) Heavy metal-regulated new microRNAs from rice. J Inorg Biochem 103:282–287

    CAS  PubMed  Google Scholar 

  • Huang SQ, Xiang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8:887–899

    CAS  PubMed  Google Scholar 

  • Huang CY, Shirley N, Genc Y, Shi B, Langridge P (2011) Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiol 156:1217–1229

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    CAS  PubMed  Google Scholar 

  • Kant S, Bi YM, Rothstein SJ (2011a) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509

    CAS  PubMed  Google Scholar 

  • Kant S, Peng M, Rothstein SJ (2011b) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to-shoot 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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Kehr J (2013) Systemic regulation of mineral homeostasis by microRNAs. Front Plant Sci 4:145

    PubMed Central  PubMed  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK (2003) Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants. Plant J 36:780–793

    CAS  PubMed  Google Scholar 

  • Kong WW, Yang ZM (2010) Identification of iron-deficiency responsive microRNA genes and cis-elements in Arabidopsis. Plant Physiol Biochem 48:153–159

    CAS  PubMed  Google Scholar 

  • Kraiser T, Gras DE, Gutiérrez AG, González B, Gutiérrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kuo HF, Chiou TJ (2011) The role of microRNAs in phosphorus deficiency signaling. Plant Physiol 156:1016–1024

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lewandowska M, Sirko A (2008) Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim Pol 55:457–471

    CAS  PubMed  Google Scholar 

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Zhang Y, Shi D, Liu X, Qin J, Ge Q, Xu L, Pan X, Li W, Zhu Y, Xu J (2013) Spatial-temporal analysis of zinc homeostasis reveals the response mechanisms to acute zinc deficiency in Sorghum bicolor. New Phytol. doi:10.1111/nph.12434

    Google Scholar 

  • Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057

    CAS  PubMed  Google Scholar 

  • Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7:e48951

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lima JC, Arenhart RA, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817–2832

    CAS  PubMed  Google Scholar 

  • Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Liu Q, Zhang H (2012) Molecular identification and analysis of arsenite stress-responsive miRNAs in rice. J Agric Food Chem 60:6524–6536

    CAS  PubMed  Google Scholar 

  • Liu TY, Chang CY, Chiou TJ (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319

    CAS  PubMed  Google Scholar 

  • Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P (2010) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62:508–517

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232

    CAS  PubMed  Google Scholar 

  • Lundmark M, Korner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140:57–68

    CAS  PubMed  Google Scholar 

  • Macovei A, Gill SS, Tuteja N (2012) microRNAs as promising tools for improving stress tolerance in rice. Plant Signal Behav 7:1296–1301

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marín-González E, Suárez-López P (2012) “And yet it moves”: cell-to-cell and long-distance signaling by plant microRNAs. Plant Sci 196:18–30

    PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matthewman CA, Kawashima CG, Huska D, Csorba T, Dalmay T, Kopriva S (2012) miR395 is a general component of the sulfate assimilation regulatory network in Arabidopsis. FEBS Lett 586:3242–3248

    CAS  PubMed  Google Scholar 

  • McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1125

    CAS  PubMed  Google Scholar 

  • Mendoza-Soto AB, Sanchez F, Hernandez G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:105

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meng YJ, Ma XX, Chen DJ, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349

    CAS  PubMed  Google Scholar 

  • Nischal L, Mohsin M, Khan I, Kardam H, Wadhwa A, Abrol YP, Iqbal M, Ahmad A (2012) Identification and comparative analysis of microRNAs associated with low-N tolerance in rice genotypes. PLoS ONE 7:e50261

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Wasaki J (2010) Recent progress in plant nutrition research: cross-talk between nutrients, plant physiology and soil microorganisms. Plant Cell Physiol 51:1255–1264

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  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

    PubMed Central  PubMed  Google Scholar 

  • Pei L, Jin Z, Li K, Yin H, Wang J, Yang A (2013) Identification and comparative analysis of low phosphate tolerance-associated microRNAs in two maize genotypes. Plant Physiol Biochem 70:221–234

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    CAS  Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    CAS  Google Scholar 

  • 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

    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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66

    CAS  PubMed  Google Scholar 

  • Sha A, Chen Y, Ba H, Shan Z, Zhang X, Wu X, Qiu D, Chen S, Zhou X (2012) Identification of Glycine max microRNAs in response to phosphorus deficiency. J Plant Biol 55:268–280

    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

    CAS  PubMed  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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:e1001031

    PubMed Central  PubMed  Google Scholar 

  • Trevisan S, Nonis A, Begheldo M, Manoli A, Palme K, Caporale G, Ruperti B, Quaggiotti S (2012) Expression and tissue-specific localization of nitrate-responsive miRNAs in roots of maize seedlings. Plant Cell Environ 35:1137–1155

    CAS  PubMed  Google Scholar 

  • Tsay YF, Ho CH, Chen HY, Lin SH (2011) Integration of nitrogen and potassium signaling. Annu Rev Plant Biol 62:207–226

    CAS  PubMed  Google Scholar 

  • Valdes-Lopez O, Arenas-Huertero C, Ramirez M, Girard L, Sanchez F, Vance CP, Luis Reyes J, Hernandez G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ 31:1834–1843

    CAS  PubMed  Google Scholar 

  • Valdes-Lopez O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernandez G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818

    CAS  PubMed  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    CAS  PubMed  Google Scholar 

  • Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451–476

    CAS  PubMed  Google Scholar 

  • Wang C, Huang W, Ying Y, Li S, Secco D, Tyerman S, Whelan J, Shou H (2012) Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves. New Phytol 196:139–148

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhang C, Hao Q, Sha A, Zhou R, Zhou X, Yuan L (2013) Elucidation of miRNAs-mediated responses to low nitrogen stress by deep sequencing of two soybean genotypes. PLoS One 8:e67423

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waters BM, McInturf SA, Stein RJ (2012) Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 63:5903–5918

    CAS  PubMed  Google Scholar 

  • Wu G (2013) Plant microRNAs and development. J Genet Genomics 40:217–230

    CAS  PubMed  Google Scholar 

  • Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi Y, Xie C (2011) Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS ONE 6:e28009

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    CAS  PubMed  Google Scholar 

  • Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14:66

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378

    CAS  PubMed  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang ZM, Chen J (2013) A potential role of microRNAs in plant response to metal toxicity. Metallomics. doi:10.1039/c3mt00022b

    Google Scholar 

  • Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297

    CAS  PubMed  Google Scholar 

  • Zeng QY, Yang CY, Ma QB, Li XP, Dong WW, Nian H (2012) Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol 12:182

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang LW, Song JB, Shu XX, Zhang Y, Yang ZM (2013) miR395 is involved in detoxification of cadmium in Brassica napus. J Hazard Mater 250–251:204–211

    PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li WX (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7:e29669

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao X, Liu X, Guo C, Gu J, Xiao K (2013a) Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol 22:113–123

    CAS  Google Scholar 

  • Zhao Y, Xu Z, Mo Q, Zou C, Li W, Xu Y, Xie C (2013b) Combined small RNA and degradome sequencing reveals novel miRNAs and their targets in response to low nitrate availability in maize. Ann Bot 112:633–642

    CAS  PubMed  Google Scholar 

  • Zhou M, Luo H (2013) MicroRNA-mediated gene regulation: potential applications for plant genetic engineering. Plant Mol Biol. doi:10.1007/s11103-013-0089-1

    Google Scholar 

  • Zhou ZS, Song JB, Yang ZM (2012a) Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 63:4597–4613

    CAS  PubMed  Google Scholar 

  • Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012b) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99

    PubMed  Google Scholar 

  • Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM (2010) microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 178:23–29

    CAS  Google Scholar 

  • Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We apologize to the authors whose work is not cited here due to space limitation. We thank Professor Zhi Min Yang for his critical reading of the manuscript and valuable comments. Our current research is supported by grants from the National Science Foundation of China (31201679 and U1130304) and the Program of New Century Excellent Talent in Universities (NCET-11-0672).

Author information

Authors and Affiliations

  1. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 310036, People’s Republic of China

    Houqing Zeng, Guoping Wang, Xiaoyan Hu, Huizhong Wang & Liqun Du

  2. College of Resource and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Yiyong Zhu

Authors
  1. Houqing Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guoping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoyan Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huizhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liqun Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yiyong Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Houqing Zeng or Yiyong Zhu.

Additional information

Responsible Editor: Philip John White.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, H., Wang, G., Hu, X. et al. Role of microRNAs in plant responses to nutrient stress. Plant Soil 374, 1005–1021 (2014). https://doi.org/10.1007/s11104-013-1907-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1907-6

Keywords

Search

Navigation