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Signaling by MicroRNAs in Response to Abiotic Stress

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Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 1

Abstract

In order to contend with different environmental adversities, plants have developed a series of mechanisms at the physiological, cellular and molecular level. Small RNA molecules known as microRNAs (miRNAs) are important regulators of gene expression in plants and animals. MicroRNAs are involved in plant development, response to hormones and environmental stress in plants.

MicroRNAs are processed from longer RNA precursors by Dicer-like enzymes to generate 20–24 nucleotide long RNA. Within a multiprotein complex called RISC (RNA-Induced Silencing Complex), the microRNA recognizes a target mRNA by RNA:RNA base-pairing. ARGONAUTE 1 is the effector protein of the RISC complex where mRNA expression is inhibited by RNA cleavage or alternatively, by translation inhibition. How the microRNA biogenesis machinery is affected by stress conditions is only beginning to be understood.

The advent of high-throughput sequencing of small RNAs has yielded a large amount of information on the miRNA landscape of many different plant species, however little is known about miRNA functions in plants other than Arabidopsis (especially crop species) and in particular their involvement in responses to external stimuli. In spite of this, many research groups have focused on how microRNAs work in relevant crops, including legumes, and their advancement may reveal novel mechanisms involved in the plant responses to different abiotic stresses. The microRNAs found in these plant species have shown novel features worth of their study: they may give rise to siRNAs (another class of non-coding small RNAs); some microRNAs* accumulate to detectable levels under certain types of abiotic stress conditions or multiple small microRNAs originate from the same precursors. These findings suggest there is a wide landscape of unknown functions for microRNAs in plants. In addition, other factors should be considered to have a better and more complete picture of microRNA functions such as the half-life of the microRNA target and the microRNA itself; competition between coding and non-coding transcripts for miRNA binding; the way in which spatial, temporal and condition-specific expression of both target and microRNA is achieved; the birth of new miRNAs during evolution and their incorporation into novel regulatory pathways. Any of these factors may have a distinct contribution given particular plant situations and/or evolutionary histories. Their understanding is crucial for a full comprehension of microRNA functionality, especially in the context of abiotic stress.

We have just started to uncover how microRNAs contribute to stress signaling and responses, however much remains to be learned and the near future promises great surprises that will contribute to a better understanding of the responses to abiotic stress, particularly, in crops.

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References

  • Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762

    Article  PubMed  CAS  Google Scholar 

  • Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ (2009) Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15:2112–2121

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Arvey A, Larsson E, Sander C, Leslie CS, Marks DS (2010) Target mRNA abundance dilutes microRNA and siRNA activity. Mol Syst Biol 6:363

    Article  PubMed  Google Scholar 

  • Axtell MJ, Westholm JO, Lai EC (2011) Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221

    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 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933

    Article  PubMed  CAS  Google Scholar 

  • Bologna NG, Mateos JL, Bresso EG, Palatnik JF (2009) A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J 28:3646–3656

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Capitao C, Paiva JA, Santos DM, Fevereiro P (2011) In Medicago truncatula, water deficit modulates the transcript accumulation of components of small RNA pathways. BMC Plant Biol 11:79

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2010) Small RNAs - secrets and surprises of the genome. Plant J 61:941–958

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Wang T, Zhao M, Tian Q, Zhang WH (2011a) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235(2):375–386

    Article  PubMed  Google Scholar 

  • Chen L, Zhang Y, Ren Y, Xu J, Zhang Z, Wang Y (2011b) Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochem Biophys Res Commun 417(2):892–896

    Article  PubMed  Google Scholar 

  • Contreras-Cubas C, Rabanal FA, Arenas-Huertero C, Ortiz MA, Covarrubias AA, Reyes JL (2012) The Phaseolus vulgaris miR159a precursor encodes a second differentially expressed microRNA. Plant Mol Biol 80:103–115

    Article  PubMed  CAS  Google Scholar 

  • Devers EA, Branscheid A, May P, Krajinski F (2011) Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol 156:1990–2010

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci USA 105:9970–9975

    Article  PubMed  CAS  Google Scholar 

  • Earley K, Smith M, Weber R, Gregory B, Poethig R (2010) An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana. Silence 1:15

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26:941–946

    Article  PubMed  CAS  Google Scholar 

  • Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461

    Article  PubMed  CAS  Google Scholar 

  • Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim F, Rymarquis LA, Kim EJ, Becker J, Balassa E, Green PJ, Cerutti H (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc Natl Acad Sci USA 107:3906–3911

    Article  PubMed  CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23(12):4185–4207

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW (2011) Conservation and divergence in plant microRNAs. Plant Mol Biol 80(1):3–16

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Yang JY, Xu J, Jang IC, Prigge MJ, Chua NH (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary MicroRNAs. Plant Cell Physiol 49:1634–1644

    Article  PubMed  CAS  Google Scholar 

  • Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimaraes FC (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307

    Article  PubMed  CAS  Google Scholar 

  • Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758

    Article  PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858

    Article  PubMed  CAS  Google Scholar 

  • Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crete P, Voinnet O, Robaglia C (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21(6):1762–1768

    Article  PubMed  CAS  Google Scholar 

  • Larsson E, Sander C, Marks D (2010) mRNA turnover rate limits siRNA and microRNA efficacy. Mol Syst Biol 6:433

    PubMed  CAS  Google Scholar 

  • Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862

    Article  PubMed  CAS  Google Scholar 

  • Laubinger S, Zeller G, Henz SR, Buechel S, Sachsenberg T, Wang JW, Ratsch G, Weigel D (2010) Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome. Proc Natl Acad Sci USA 107:17466–17473

    Article  PubMed  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62:742–759

    Article  PubMed  CAS  Google Scholar 

  • Li B, Qin Y, Duan H, Yin W, Xia X (2011a) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  PubMed  CAS  Google Scholar 

  • Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011b) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11:170

    Article  PubMed  Google Scholar 

  • Li Y, Li C, Ding G, Jin Y (2011c) Evolution of MIR159/319 microRNA genes and their post-transcriptional regulatory link to siRNA pathways. BMC Evol Biol 11:122

    Article  PubMed  CAS  Google Scholar 

  • Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002a) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002b) Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366

    PubMed  CAS  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151

    Article  PubMed  CAS  Google Scholar 

  • Mateos JL, Bologna NG, Chorostecki U, Palatnik JF (2010) Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr Biol 20:49–54

    Article  PubMed  CAS  Google Scholar 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell 133:116–127

    Article  PubMed  CAS  Google Scholar 

  • Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141

    Article  PubMed  CAS  Google Scholar 

  • Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3' UTR evolution. Nat Struct Mol Biol 15:354–363

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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 

  • Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976

    PubMed  CAS  Google Scholar 

  • Papp I, Mur LA, Dalmadi A, Dulai S, Koncz C (2004) A mutation in the cap binding protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol Biol 55:679–686

    Article  PubMed  CAS  Google Scholar 

  • Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–2242

    Article  PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696

    Article  PubMed  CAS  Google Scholar 

  • Qian Y, Cheng Y, Cheng X, Jiang H, Zhu S, Cheng B (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30:1347–1363

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran V, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–1492

    Article  PubMed  CAS  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  PubMed  CAS  Google Scholar 

  • Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146:353–358

    Article  PubMed  CAS  Google Scholar 

  • Song L, Axtell MJ, Fedoroff NV (2010) RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr Biol 20:37–41

    Article  PubMed  CAS  Google Scholar 

  • Song QX, Liu YF, Hu XY, Zhang WK, Ma B, Chen SY, Zhang JS (2011) Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 11:5

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13:350–358

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 8:1187–1197

    Article  Google Scholar 

  • Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351

    PubMed  CAS  Google Scholar 

  • Vazquez F, Legrand S, Windels D (2010) The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci 15:337–345

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367

    Article  PubMed  CAS  Google Scholar 

  • Werner S, Wollmann H, Schneeberger K, Weigel D (2010) Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr Biol 20:42–48

    Article  PubMed  CAS  Google Scholar 

  • Wong CE, Zhao YT, Wang XJ, Croft L, Wang ZH, Haerizadeh F, Mattick JS, Singh MB, Carroll BJ, Bhalla PL (2011) MicroRNAs in the shoot apical meristem of soybean. J Exp Bot 62:2495–2506

    Article  PubMed  CAS  Google Scholar 

  • Yan Y, Zhang Y, Yang K, Sun Z, Fu Y, Chen X, Fang R (2011) Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J 65:820–828

    Article  PubMed  CAS  Google Scholar 

  • Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850

    Article  PubMed  CAS  Google Scholar 

  • Yin Z, Li Y, Yu J, Liu Y, Li C, Han X, Shen F (2011) Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol Biol Rep 39(4):4961–4970

    Article  PubMed  Google Scholar 

  • Yoo BC, 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

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Bi L, Zheng B, Ji L, Chevalier D, Agarwal M, Ramachandran V, Li W, Lagrange T, Walker JC (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci USA 105:10073–10078

    Article  PubMed  CAS  Google Scholar 

  • Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, Gonzalez AJ, Yan Z, Kitto SL, Grusak MA (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    Article  PubMed  CAS  Google Scholar 

  • Zhang JF, Yuan LJ, Shao Y, Du W, Yan DW, Lu YT (2008) The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant Cell Environ 31:562–574

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Gao S, Zhou X, Xia J, Chellappan P, Zhang X, Jin H (2010) Multiple distinct small RNAs originate from the same microRNA precursors. Genome Biol 11:R81

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Expt Bot 61:4157–4168

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

G. S.-V. received a PhD scholarship from CONACyT. Work on microRNAs in the laboratory of the authors is partially supported by grants from DGAPA-PAPIIT (IN-205112) and CONACyT (CB2010-151571) to JLR.

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Correspondence to José Luis Reyes .

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Sosa-Valencia, G., Covarrubias, A.A., Reyes, J.L. (2013). Signaling by MicroRNAs in Response to Abiotic Stress. In: Sarwat, M., Ahmad, A., Abdin, M. (eds) Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 1. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6372-6_3

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