Abiotic stress-associated microRNAs in plants: discovery, expression analysis, and evolution

Abstract

Abiotic stresses such as drought, cold, and high salinity are among the most adverse factors that affect plant growth and yield in the field. MicroRNAs are small RNA molecules that regulate gene expression in a sequence-specific manner and play an important role in plant stress response. Identifying abiotic stress-associated microRNAs and understanding their function will help develop new strategies for improvement of plant stress tolerance. Here we highlight recent advances in our understanding of abiotic stress-associated miRNAs in various plants, with focus on their discovery, expression analysis, and evolution.

Keywords

microRNA / abiotic stress / epigenetics / gene expression / evolution

References

[1] Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V (2005). Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res, 15(1): 78–91

[2] Addo-Quaye C, Eshoo T W, Bartel D P, Axtell M J (2008). Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol, 18(10): 758–762

[3] Allen E, Xie Z, Gustafson A M, Carrington J C (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121(2): 207–221

[4] Allen E, Xie Z, Gustafson A M, Sung G H, Spatafora J W, Carrington J C (2004). Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet, 36(12): 1282–1290

[5] Ambros V, Bartel B, Bartel D P, Burge C B, Carrington J C, Chen X, Dreyfuss G, Eddy S R, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003). A uniform system for microRNA annotation. RNA, 9(3): 277–279

[6] Audic S, Claverie J M (1997). The significance of digital gene expression profiles. Genome Res, 7(10): 986–995

[7] Axtell M J, Bowman J L (2008). Evolution of plant microRNAs and their targets. Trends Plant Sci, 13(7): 343–349

[8] Axtell M J, Snyder J A, Bartel D P (2007). Common functions for diverse small RNAs of land plants. Plant Cell, 19(6): 1750–1769

[9] Barrera-Figueroa B E, Gao L, Diop N N, Wu Z, Ehlers J D, Roberts P A, Close T J, Zhu J K, Liu R (2011). Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol, 11(1): 127

[10] Bartel D P (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2): 281–297

[11] Bonnet E, Wuyts J, Rouzé P, Van de Peer Y (2004). Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci USA, 101(31): 11511–11516

[12] Borsani O, Zhu J, Verslues P E, Sunkar R, Zhu J K (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell, 123(7): 1279–1291

[13] Boyer J S (1982). Plant productivity and environment. Science, 218(4571): 443–448

[14] Bureau T E, Wessler S R (1992). Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell, 4(10): 1283–1294

[15] Chen C, Tan R, Wong L, Fekete R, Halsey J (2011). Quantitation of microRNAs by real-time RT-qPCR. Methods Mol Biol, 687: 113–134

[16] Chen X (2005). MicroRNA biogenesis and function in plants. FEBS Lett, 579(26): 5923–5931

[17] Chinnusamy V, Zhu J K (2009). RNA-directed DNA methylation and demethylation in plants. Sci China C Life Sci, 52(4): 331–343

[18] Chiou T J, Aung K, Lin S I, Wu C C, Chiang S F, Su C L (2006). Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell, 18(2): 412–421

[19] Cuperus J T, Fahlgren N, Carrington J C (2011). Evolution and functional diversification of MIRNA genes. Plant Cell, 23(2): 431–442

[20] Dai X, Zhuang Z, Zhao P X (2011). Computational analysis of miRNA targets in plants: current status and challenges. Brief Bioinform, 12(2): 115–121

[21] Dalmay T (2006). Short RNAs in environmental adaptation. Proc Biol Sci, 273(1594): 1579–1585

[22] Devers E A, Branscheid A, May P, Krajinski F (2011). Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in Arbuscular mycorrhizal symbiosis. Plant Physiol, 156(4): 1990–2010

[23] Dezulian T, Remmert M, Palatnik J F, Weigel D, Huson D H (2006). Identification of plant microRNA homologs. Bioinformatics, 22(3): 359–360

[24] Ding Y, Chen Z, Zhu C (2011). Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot, 62(10): 3563–3573

[25] Fahlgren N, Howell M D, Kasschau K D, Chapman E J, Sullivan C M, Cumbie J S, Givan S A, Law T F, Grant S R, Dangl J L, Carrington J C (2007). High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE, 2(2): e219

[26] Fahlgren N, Jogdeo S, Kasschau K D, Sullivan C M, Chapman E J, Laubinger S, Smith L M, Dasenko M, Givan S A, Weigel D, Carrington J C (2010). MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell, 22(4): 1074–1089

[27] Felippes F F, Schneeberger K, Dezulian T, Huson D H, Weigel D (2008). Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA, 14(12): 2455–2459

[28] Ge Y, Li Y, Zhu Y M, Bai X, Lv D K, Guo D, Ji W, Cai H (2010). Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol, 10(1): 153

[29] German M A, Pillay M, Jeong D H, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis L A, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers B C, Green P J (2008). Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol, 26(8): 941–946

[30] Gou J Y, Felippes F F, Liu C J, Weigel D, Wang J W (2011). Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell, 23(4): 1512–1522

[31] Jacob F, Monod J (1961). Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol, 3(3): 318–356

[32] Jia X, Wang W X, Ren L, Chen Q J, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009). Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol, 71(1-2): 51–59

[33] Jiang N, Feschotte C, Zhang X, Wessler S R (2004). Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol, 7(2): 115–119

[34] Jin H, Vacic V, Girke T, Lonardi S, Zhu J K (2008). Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis. BMC Mol Biol, 9(1): 6

[35] Johnson C, Bowman L, Adai A T, Vance V, Sundaresan V (2007). CSRDB: a small RNA integrated database and browser resource for cereals. Nucleic Acids Res, 35(Database Database issue): D829–D833

[36] Jones-Rhoades M W, Bartel D P (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell, 14(6): 787–799

[37] Jones-Rhoades M W, Bartel D P, Bartel B (2006). MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol, 57(1): 19–53

[38] Joung J G, Fei Z (2009). Identification of microRNA regulatory modules in Arabidopsis via a probabilistic graphical model. Bioinformatics, 25(3): 387–393

[39] Kantar M, Lucas S J, Budak H (2011). miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta, 233(3): 471–484

[40] Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007). A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev, 21(23): 3123–3134

[41] Langmead B, Trapnell C, Pop M, Salzberg S L (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol, 10(3): R25

[42] Lau N C, Lim L P, Weinstein E G, Bartel D P (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science, 294(5543): 858–862

[43] Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009). Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell, 21(9): 2780–2796

[44] 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(11): 3765–3779

[45] Li R, Yu C, Li Y, Lam T W, Yiu S M, Kristiansen K, Wang J (2009). SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics, 25(15): 1966–1967

[46] Li W X, Oono Y, Zhu J, He X J, Wu J M, Iida K, Lu X Y, Cui X, Jin H, Zhu J K (2008). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell, 20(8): 2238–2251

[47] Li Y, Li C, Xia J, Jin Y (2011b). Domestication of transposable elements into MicroRNA genes in plants. PLoS ONE, 6(5): e19212

[48] Li Y F, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell M J, Zhang W, Sunkar R (2010). Transcriptome-wide identification of microRNA targets in rice. Plant J, 62(5): 742–759

[49] Lindow M, Krogh A (2005). Computational evidence for hundreds of non-conserved plant microRNAs. BMC Genomics, 6(1): 119

[50] Liu B, Liu L, Tsykin A, Goodall G J, Green J E, Zhu M, Kim C H, Li J (2010). Identifying functional miRNA-mRNA regulatory modules with correspondence latent dirichlet allocation. Bioinformatics, 26(24): 3105–3111

[51] Liu H H, Tian X, Li Y J, Wu C A, Zheng C C (2008). Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14(5): 836–843

[52] Llave C, Franco-Zorrilla J M, Solano R, Barajas D (2011). Target validation of plant microRNAs. Methods Mol Biol, 732: 187–208

[53] Llave C, Kasschau K D, Rector M A, Carrington J C (2002). Endogenous and silencing-associated small RNAs in plants. Plant Cell, 14(7): 1605–1619

[54] Lu C, Jeong D H, Kulkarni K, Pillay M, Nobuta K, German R, Thatcher S R, Maher C, Zhang L, Ware D, Liu B, Cao X, Meyers B C, Green P J (2008a). Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA, 105(12): 4951–4956

[55] Lu C, Kulkarni K, Souret F F, MuthuValliappan R, Tej S S, Poethig R S, Henderson I R, Jacobsen S E, Wang W, Green P J, Meyers B C (2006). MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res, 16(10): 1276–1288

[56] Lu C, Meyers B C, Green P J (2007). Construction of small RNA cDNA libraries for deep sequencing. Methods, 43(2): 110–117

[57] Lu C, Tej S S, Luo S J, Haudenschild C D, Meyers B C, Green P J (2005a). Elucidation of the small RNA component of the transcriptome. Science, 309(5740): 1567–1569

[58] Lu S, Sun Y H, Chiang V L (2008b). Stress-responsive microRNAs in Populus. Plant J, 55(1): 131–151

[59] Lu S, Sun Y H, Shi R, Clark C, Li L, Chiang V L (2005b). Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell, 17(8): 2186–2203

[60] McCormick K P, Willmann M R, Meyers B C (2011). Experimental design, preprocessing, normalization and differential expression analysis of small RNA sequencing experiments. Silence, 2(1): 2

[61] Megraw M, Baev V, Rusinov V, Jensen S T, Kalantidis K, Hatzigeorgiou A G (2006). MicroRNA promoter element discovery in Arabidopsis. RNA, 12(9): 1612–1619

[62] Mendes N D, Freitas A T, Sagot M F (2009). Current tools for the identification of miRNA genes and their targets. Nucleic Acids Res, 37(8): 2419–2433

[63] Meng Y, Shao C, Chen M (2011). Toward microRNA-mediated gene regulatory networks in plants. Brief Bioinform, 12(6): 645–659

[64] Meyers B C, Axtell M J, Bartel B, Bartel D P, Baulcombe D, Bowman J L, Cao X, Carrington J C, Chen X, Green P J, Griffiths-Jones S, Jacobsen S E, Mallory A C, Martienssen R A, Poethig R S, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu J K (2008). Criteria for annotation of plant MicroRNAs. Plant Cell, 20(12): 3186–3190

[65] Nobuta K, Venu R C, Lu C, Beló A, Vemaraju K, Kulkarni K, Wang W Z, Pillay M, Green P J, Wang G L, Meyers B C (2007). An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol, 25(4): 473–477

[66] Pak J, Fire A (2007). Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science, 315(5809): 241–244

[67] 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(6): 960–976

[68] Piriyapongsa J, Jordan I K (2008). Dual coding of siRNAs and miRNAs by plant transposable elements. RNA, 14(5): 814–821

[69] Pradervand S, Weber J, Lemoine F, Consales F, Paillusson A, Dupasquier M, Thomas J, Richter H, Kaessmann H, Beaudoing E, Hagenbüchle O, Harshman K (2010). Concordance among digital gene expression, microarrays, and qPCR when measuring differential expression of microRNAs. Biotechniques, 48(3): 219–222

[70] Rajagopalan R, Vaucheret H, Trejo J, Bartel D P (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev, 20(24): 3407–3425

[71] Reinhart B J, Bartel D P (2002). Small RNAs correspond to centromere heterochromatic repeats. Science, 297(5588): 1831

[72] Rhoades M W, Reinhart B J, Lim L P, Burge C B, Bartel B, Bartel D P (2002). Prediction of plant microRNA targets. Cell, 110(4): 513–520

[73] Robinson M D, McCarthy D J, Smyth G K (2010). EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1): 139–140

[74] Ron M, Alandete Saez M, Eshed Williams L, Fletcher J C, McCormick S (2010). Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev, 24(10): 1010–1021

[75] Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J, 31(3): 279–292

[76] Song Q X, Liu Y F, Hu X Y, Zhang W K, Ma B, Chen S Y, Zhang J S (2011). Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol, 11(1): 5

[77] Sunkar R, Girke T, Jain P K, Zhu J K (2005). Cloning and characterization of microRNAs from rice. Plant Cell, 17(5): 1397–1411

[78] Sunkar R, Jagadeeswaran G (2008). In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol, 8(1): 37

[79] Sunkar R, Kapoor A, Zhu J K (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(8): 2051–2065

[80] Sunkar R, Zhou X F, Zheng Y, Zhang W X, Zhu J K (2008). Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol, 8(1): 25

[81] Sunkar R, Zhu J K (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16(8): 2001–2019

[82] Szittya G, Moxon S, Santos D M, Jing R, Fevereiro M P, Moulton V, Dalmay T (2008). High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics, 9(1): 593

[83] Valdés-López O, Yang S S, Aparicio-Fabre R, Graham P H, Reyes J L, Vance C P, Hernández G (2010). MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol, 187(3): 805–818

[84] Vaucheret H (2006). Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev, 20(7): 759–771

[85] Vazquez F, Legrand S, Windels D (2010). The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci, 15(6): 337–345

[86] Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory A C, Hilbert J L, Bartel D P, Crété P (2004). Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell, 16(1): 69–79

[87] Vigneault F, Sismour A M, Church G M (2008). Efficient microRNA capture and bar-coding via enzymatic oligonucleotide adenylation. Nat Methods, 5(9): 777–779

[88] Wang X J, Reyes J L, Chua N H, Gaasterland T (2004). Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol, 5(9): R65

[89] Wei B, Cai T, Zhang R, Li A, Huo N, Li S, Gu Y Q, Vogel J, Jia J, Qi Y, Mao L (2009). Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomics, 9(4): 499–511

[90] Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009). Rice MicroRNA effector complexes and targets. Plant Cell, 21(11): 3421–3435

[91] Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010). DNA methylation mediated by a microRNA pathway. Mol Cell, 38(3): 465–475

[92] Xie Z, Allen E, Fahlgren N, Calamar A, Givan S A, Carrington J C (2005). Expression of Arabidopsis MIRNA genes. Plant Physiol, 138(4): 2145–2154

[93] Xuan P, Guo M, Liu X, Huang Y, Li W, Huang Y (2011). PlantMiRNAPred: efficient classification of real and pseudo plant pre-miRNAs. Bioinformatics, 27(10): 1368–1376

[94] Zhang B H, Pan X P, Cannon C H, Cobb G P, Anderson T A (2006). Conservation and divergence of plant microRNA genes. Plant J, 46(2): 243–259

[95] Zhang J Y, Xu Y Y, Huan Q, Chong K (2009a). Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics, 10(1): 449

[96] Zhang L F, Chia J M, Kumari S, Stein J C, Liu Z J, Narechania A, Maher C A, Guill K, McMullen M D, Ware D (2009b). A genome-wide characterization of microRNA genes in maize. PLoS Genet, 5(11): e1000716

[97] Zhao M, Ding H, Zhu J K, Zhang F, Li W X (2011). Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol, 190(4): 906–915

[98] Zhu J K (2002). Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 53(1): 247–273

[99] Zhu Q H, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008). A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res, 18(9): 1456–1465

Acknowledgments

This work was supported in part by a USDA hatch fund (CA-R*-BPS-7754-H) to RL.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg