Abstract
Drought is a major environmental stress factor that affects plant growth and development worldwide. Wild emmer wheat (Triticum turgidum ssp. dicoccoides), the ancestor of domesticated durum wheat (Triticum turgidum ssp. durum), has great potential for improving the understanding of the wheat drought response. MicroRNAs (miRNAs) are a recently discovered class of gene expression regulators that have also been linked to several plant stress responses; however, this relationship is just beginning to be understood. miRNA expression patterns of drought-resistant wild emmer wheat in response to drought stress were investigated using a plant miRNA microarray platform. Expression was detected to be 205 miRNAs in control and 438 miRNAs in drought-stressed leaf and root tissues. Of these miRNAs, the following 13 were differentially regulated in response to drought: miR1867, miR896, miR398, miR528, miR474, miR1450, miR396, miR1881, miR894, miR156, miR1432, miR166 and miR171. Regulation of miRNAs upon 4 and 8 h drought stress applications observed by qRT-PCR. Target transcripts of differentially regulated miRNAs were computationally predicted. In addition to miRNA microarray study, five new conserved T. turgidum miRNAs were identified through a homology-based approach, and their secondary structures and putative targets were predicted. These findings both computationally and experimentally highlight the presence of miRNAs in T. dicoccoides and further extend the role of miRNAs under shock drought stress conditions.
Similar content being viewed by others
Abbreviations
- miRNA:
-
MicroRNA
- mRNA:
-
Messenger RNA
- MFEI:
-
Minimum folding free energy index
- EST:
-
Expressed seqeunce tag
- ABA:
-
Abscisic acid
- GRL:
-
Growth factor-like transcription factor
- PDH:
-
Proline dehydrogenase
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
Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741
Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
Budak H, Kasap Z, Shearman RC, Dweikat I, Sezerman U, Mahmood A (2006) Molecular characterization of cDNA encoding resistance gene-like sequences in Buchloe dactyloides. Mol Biotech 34:293–301
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338
Cebeci O, Budak H (2009) Global expression patterns of three Festuca species exposed to different doses of glyphosate using the affymetrix genechip wheat genome array. Comp Funct Genomics 2009:505701
Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931
Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147:469–486
Covarrubias AA, Reyes JL (2010) Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant Cell Environ 33:481–489
Dryanova A, Zekharov A, Gulick PJ (2008) Data mining for miRNAs and their targets in the Triticeae. Genome 51:433–443
Dugas DV, Bartel B (2004) MicroRNA regulation of gene expression in plants. Curr Opin Plant Biol 7:512–520
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868
Ergen NZ, Budak H (2009) Sequencing over 13,000 expressed sequence tags from six subtractive cDNA libraries of wild and modern wheats following slow drought stress. Plant Cell Environ 32:220–236
Ergen NZ, Dinler G, Shearman RC, Budak H (2007) Identifiying, cloning and structural analysis of differentially expressed genes upon Puccinia infection of Festuca rubra var rubra. Gene 393:145–152
Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics 9:377–396
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
Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144
Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D140–D144
Jia X, Wang WX, Ren L, Chen QJ, 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 71:51–59
Jin W, Li N, Zhang B, Wu F, Li W, Guo A, Deng Z (2008) Identification and verification of microRNA in wheat (Triticum aestivum). J Plant Res 121:351–355
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) Micro-RNA mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNA upon dehydration stress correlated with target gene expression. Funct Integr Genomics. doi:10.1007/s10142-010-0181-4
Lee Y, Tsai J, Sunkara S, Karamycheva S, Pertea G, Sultana R, Antonescu V, Chan A, Cheung F, Quackenbush J (2005) The TIGR gene ındices: clustering and assembling EST and known genes and integration with eukaryotic genomes. Nucleic Acids Res 33:D71–D74
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
Liu D, Yu D (2009) MicroRNA (miR396) negatively regulates the expression of ceramidase genes in Arabidopsis. Prog Nat Sci 19:781–785
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843
Llave C, Kasschau KD, Rector MA, Carrington JC (2002a) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619
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
Lu S, SunYH Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203
Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis auxin response factor 17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375
Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940
Nishimura N, Kitahata N, Seki M, Narusaka Y, Narusaka M, Kuromori T, Asami T, Shinozaki K, Hirayama T (2005) Analysis of ABA Hypersensitive Germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984
Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263
Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470
Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2010.04.001
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miRNA398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066
Thomson JM, Parker J, Perou CM, Hammond SM (2004) A custom microarray platform for analysis of microRNA gene expression. Nat Methods 1:47–53
Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Bracyhpodium distachyon. Planta 230:659–669
Unver T, Namuth-Covert DM, Budak H (2009) Review of current methodological approaches for characterizing microRNAs in plants. Int J Plant Genomics. doi:10.1155/2009/262463
Unver T, Bakar M, Shearman RC, Budak H (2010) Genome-wide profiling and analysis of Festuca arundinacea miRNAs and transcriptomes in response to foliar glyphosate application. Mol Genet Genomics 283:397–413
Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12. doi:10.1186/1746-4811-3-12
Vaucheret H, Vazquez F, Crété 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 18:1187–1197
Wei B, Cai T, Zhang R, Li A, Huo N, Li S, Gu YQ, Vogel J, Jia J, Qi Y, Mao L (2009a) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomics 9:499–511
Wei L, Zhang D, Xiang F, Zhang Z (2009b) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547
Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123
Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1:771–781
Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8:R96
Yao Y, Ni Z, Peng H, Sun F, Xin M, Sunkar R, Zhu JK, Sun Q (2010) Non-coding small RNAs responsive to abiotic stress in wheat (Triticum aestivum L.). Funct Integr Genomics 10:187–190
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214
Zhang BH, Pan XP, Cobb GP, Anderson TA (2006a) Plant microRNA: a small regulatory molecule with a big impact. Dev Biol 289:3–16
Zhang BH, Pan XP, Cobb GP, Anderson TA (2006b) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63:246–254
Zhang BH, Pan XP, Stellwag EJ (2008) Identification of soybean microRNAs and their targets. Planta 229:161–182
Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Bioph Res Commun 354:585–590
Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103. doi:10.1038/msb4100143
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Author information
Authors and Affiliations
Corresponding author
Additional information
M. Kantar and S. J. Lucas regarded as joint first authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kantar, M., Lucas, S.J. & Budak, H. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233, 471–484 (2011). https://doi.org/10.1007/s00425-010-1309-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-010-1309-4