Abstract
In natural environments, plants frequently have to cope with insufficient nutrient supply, which significantly impairs crop yield. Nutrients have to be optimally distributed to permit the best possible growth and reproduction. To react to nutrient deficiencies, plants have evolved a broad spectrum of diverse metabolic, physiological and developmental adaptations. The amount and availability of different nutrients has to be monitored in individual cells and organs, and information about the nutrient status has to be communicated over short and long distances. Recent studies have shown that specific miRNAs are important components of plant responses to nutrient starvation. miR395, positively responsive to sulfur starvation, miR398, induced by low copper and sucrose, and miR399, induced by phosphate deficiency, are among the best studied nutrient-dependent miRNAs. This chapter will summarize current knowledge about the functions of these miRNAs under different nutrient deficiencies, and the possible contribution of miRNA-based regulation to maintaining nutrient homeostasis.
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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 Biochem 283:15932–15945
Abdel-Ghany SE, Burkhead JL, Gogolin KA, Andres-Colas N, Bodecker JR, Puig S, Penarrubia L, Pilon M (2005) AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett 579:2307–2312
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221
Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Aung K, Lin S, Wu C, Huang Y, Su C, Chiou T (2006) Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011
Bari R, Pant BD, Stitt M, Scheible W (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250
Bick JA, Leustek T (1998) Plant sulfur metabolism—the reduction of sulfate to sulfite. Curr Opin Plant Biol 1:240–244
Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible W, 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
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
Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64
Burke JJ, Holloway P, Dalling MJ (1986) The effect of sulfur deficiency on the organization and photosynthetic capability of wheat leaves. J Plant Physiol 125:371–375
Burleigh SH, Harrison MJ (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119:241–248
Carfagna S, Vona V, Di Martino V, Esposito S, Rigano C (2011) Nitrogen assimilation and cysteine biosynthesis in barley: evidence for root sulphur assimilation upon recovery from N deprivation. Environ Exp Bot 71:18–24
Casimiro A, Barroso J, Pais MS (1990) Effect of copper deficiency on photosynthetic electron transport in wheat plants. Physiol Plantarum 79:459–464
Chapin SF (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260
Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332
Chiou T, Aung K, Lin S, Wu C, Chiang S, Su C (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421
Cohu CM, Pilon M (2007) Regulation of superoxide dismutase expression by copper availability. Physiol Plantarum 129:747–755
Combier J, 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
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
Dan H, Yang Y, Zheng ZL (2007) A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana. Plant Mol Biol 63:221–235
Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213
Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417
Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O (2007) Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet 39:848–856
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219. doi:10.1371/journal.pone.0000219
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
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
Gao N, Yanhua S, 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 transporter. Plant Soil 334:123–136
Guo X, Gui Y, Wang Y, Zhu QH, Helliwell C, Fan L (2008) Selection and mutation on microRNA target sequences during rice evolution. BMC Genomics 9:454. doi:10.1186/1471-2164-9-454
Hardtke CS (2006) Root development—branching into novel spheres. Curr Opin Plant Biol 9:66–71
Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248:51–58
Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S‐utilization efficiency. J Exp Bot 51:131–138
Hsieh L, Lin S, Shih AC, Chen J, Lin W, Tseng C, Li W, Chiou T (2009) Uncovering small RNA-mediated responses to phosphate deficiency 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 NECROSIS 1 plays a pivotal role in regulation of multiple phosphate starvation responses in rice. Plant Physiol 156:1101–1115. doi:10.1104/pp.110.170209
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88
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
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
Kim JY, Lee HJ, Jung HJ, Maruyama K, Suzuki N, Kang H (2010) Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232:1447–1454
Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495
Kuo HF, Chiou TJ (2011) The role of microRNAs in phosphorus deficiency signaling. Plant Physiol 156(3):1016–1024. doi:10.1104/pp.111.175265
Kutz A, Müller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713
Lewis R, Mendu V, Mcnear D, Tang G (2010) Roles of microRNAs in plant abiotic stress. In: Jain SM, Brar DS (eds) Molecular techniques in crop improvement. Springer Science+Business Media B.V, Berlin, pp 357–372
Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057
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
Lin S, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil J, Breitler JC, Périn C, Ko S, Guiderdoni E, Chiou T, 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
Lindow M, Jacobsen A, Nygaard S, Mang Y, Krogh A (2007) Intragenomic matching reveals a huge potential for miRNA-mediated regulation in plants. PLoS Comput Biol 3:e238
Liu J, Vance CP (2010) Crucial roles of sucrose and microRNA399 in systemic signaling of P deficiency: A tale of two team players? Plant Signal Behav 5:1556–1560
Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–268
Liu TY, Chang CY, Chiou TJ (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319
Liu J, Allan DL, Vance CP (2010) Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Mol Plant 3:428–437
Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287
Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232
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 Plantarum 140:57–68
Marschner H (1995) Mineral nutrition of higher plants. Academic, London
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
Mendoza-Cózatl D, Butko E, Springer F, Torpey J, Komives E, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus and role for thiol-peptides in long-distance transport of cadmium. Plant J 54:249–259
Menge JA, Steirle D, Bagyaraj DJ, Johnson ELV, Leonard RT (1978) Phosphorus concentrations in plants responsible for inhibition of mycorrhizal infection. New Phytol 3:575–578
Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupine (Lupinus albus L.). Ann Bot 85:909–919
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
Nilsson L, Müller R, Nielsen TH (2010) Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol Plantarum 139:129–143
Nogueira F, Chitwood D, Madi S, Kazuhiro O, Schnable P, Scalon M, Timmermans MC (2009) Regulation of small RNA accumulation in the maize shoot apex. PLoS Genet 5:e1000320
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
Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible W (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
Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764
Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipids and NADPH‐dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84
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
Shane MW, Lambers H (2006) Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of ‘P toxicity’. J Exp Bot 57:413–423
Sunkar R, Zhu J (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Kapoor A, Zhu J (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
Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu J (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25, doi:10.1186/1471-2229-8-25
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
Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47:140–151
Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM (2010) Characterisation of microRNAs from apple (Malus domestica ’Royal Gala’) vascular tissue and phloem sap. BMC Plant Biol 10:159
Vierheilig H, Garcia-Garrido JM, Wyss U, Piche Y (2000) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595
Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170
Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by microRNA in Arabidopsis. J Biol Chem 282:16369–16378
Yamasaki H, Pilon M, Shikanai T (2008) How do plants respond to copper deficiency? Plant Signal Behav 3:231–232
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
Yoo B, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000
Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473
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The author is grateful for financial support by the Spanish Ministry of Science and Innovation (MICINN, grant BIO2008-03432 and the I3 program).
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Kehr, J. (2012). Roles of miRNAs in Nutrient Signaling and Homeostasis. In: Sunkar, R. (eds) MicroRNAs in Plant Development and Stress Responses. Signaling and Communication in Plants, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27384-1_10
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