Arabidopsis thaliana microRNA162 level is posttranscriptionally regulated via splicing and polyadenylation site selection.
AbstractArabidopsis microRNA162 level regulation was studied under abiotic stresses such as drought and salinity. The TaqMan® microRNA assay proved that A. thaliana miRNA162 level was elevated under these stresses confirming its salt and drought responsiveness. Consistently, the MIR162a and MIR162b gene promoter region analyses identified numerous salinity and drought responsive elements. However, our analyses show that generally MIR162b is rather weakly expressed, both in control and stress conditions. On the other site the stress-dependent regulation of the pri-miRNA162a alternative splicing pattern revealed the increase of functional pri-miR162a isoform and preferential distal polyA site selection in stress conditions. Apart from the potential transcriptional regulation of the miRNA genes (MIRs) expression the data obtained point to an essential role of posttranscriptional regulation of the microRNA162 level.
Agranat-Tamir L, Shomron N, Sperling J, Sperling R (2014) Interplay between pre-mRNA splicing and microRNA biogenesis within the supraspliceosome. Nucleic Acids Res 42(7): 4640-4651, doi: 10.1093/nar/gkt1413.
Ambrosone A, Costa A, Leone A, Grillo S (2012) Beyond transcription: RNA-binding proteins as emerging regulators of plant response to environmental constraints. Plant Sci 182: 12-18, doi: 10.1016/j.plantsci.2011.02.004.
Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak AM, Vazquez F, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front Plant Sci 6: 410, doi: 10.3389/fpls.2015.00410.
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281–297.
Beauclair L, Yu A, Bouché N (2010) MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62(3): 454–462, doi: 10.1111/j.1365-313X.2010.04162.x.
Bielewicz D, Dolata J, Zielezinski A, Alaba S, Szarzynska B, Szczesniak MW, Jarmolowski A, Szweykowska-Kulinska Z, Karlowski WM (2012) mirEX: a platform for comparative exploration of plant pri-miRNA expression data. Nucleic Acids Res 40:191–197, doi: 10.1093/nar/gkr878.
Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A, Vazquez F, Szweykowska-Kulinska Z, Jarmolowski A (2013) Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep 14: 622-628, doi: 10.1038/embor.2013.62.
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth Stage–Based Phenotypic Analysis of Arabidopsis: A Model for High Throughput Functional Genomics in Plants. Plant Cell 13(7): 1499–1510.
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, doi: 10.1126/science.1159151.
Brown JWS, Marshall DF, Echeverria M (2008) Intronic noncoding RNAs and splicing. Trends Plant Sci 3:7, 335-342, doi: 10.1016/j.tplants.2008.04.010.
Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 Regulates Abiotic Stress-Responsive Gene Expression by Binding to Different cis-Acting Elements in Response to Different Stress Signals. Plant Physiol 162: 1566-1582, doi: 10.1104/pp.113.221911.
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103: 29-38, doi: 10.1093/aob/mcn205.
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, doi: 10.1073/pnas.0803356105.
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, doi: 10.3390/ijms131215826.
Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093-1098.
Higo K, Ugawa Y, Iwamoto M, and Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database:1999. Nucleic Acids Res 27:1, 297-300.
Hirsch J, Lefort V, Vankersschaver M, Boualem A, Lucas A, Thermes C, d’Aubenton-Carafa Y, Crespi M (2006) Characterization of 43 Non-Protein-Coding mRNA Genes in Arabidopsis, Including the MIR162a-Derived Transcripts. Plant Physiol 140: 1192-1204.
Jia F, Rock CD (2013) MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Mol Biol 81: 447-60, http://dx.doi.org/10.1007/s11103-013-0015-6.
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
Kruszka K, Pacak A, Swida-Barteczka A, Nuc P, Alaba S, Wroblewska Z, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2014) Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. J Exp Bot 65: 6123-6135., doi: 10.1093/jxb/eru353.
Kruszka K, Pacak A, Swida-Barteczka A, Stefaniak AK, Kaja E, Sierocka I, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2013) Developmentally regulated expression and complex processing of barley pri-microRNAs. BMC Genomics 14:34, doi:10.1186/1471-2164-14-34.
Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12: 206–212.
Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, Ratsch G, Weigel D (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and micro RNA processing in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 8795–8800, doi: 10.1073/pnas.0802493105.
Liu J-X, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signalling. Plant J 51: 897-909.
Lobbes D, Rallapalli D, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7(10): 1052-1058.
Lu SF, Sun YH, Shi R, Clark C, Li LG, Chiang VL (2005) Novel and mechanical stress responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17: 2186–2203.
Manavella PA, Hagmann J, Ott F, Laubinger S, Franz M, Macek B, Weigel D (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151: 859–870, doi: 10.1016/j.cell.2012.09.039.
Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12: 1612-1619, doi: 10.1261/rna.130506.
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.
Ramalingam P, Palanichamy JK, Singh A, Das P, Bhagat M, Kassab MA, Sinha S, Chattopadhyay P (2014) Biogenesis of intronic miRNAs located in clusters by independent transcription and alternative splicing. RNA 20 (1): 76-87, doi: 10.1261/rna.041814.113.
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Gene Dev 16: 1616-1626.
Ren G, Xie M, Dou Y, Zhang C, Yu B (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109: 12817 – 12821, doi: 10.1073/pnas.1204915109.
Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25: 2383-2399, doi: http://dx.doi.org/10.1105/tpc.113.113159.
Schwab R, Speth C, Laubinger S, Voinnet O (2013) Enhanced microRNA accumulation through stemloop-adjacent introns. EMBO Rep 14: 615-621, doi: 10.1038/embor.2013.58.
Sun G, Stewart CN Jr, Xiao P, Zhang B (2012) MicroRNA Expression Analysis in the Cellulosic Biofuel Crop Switchgrass (Panicum virgatum) under Abiotic Stress. PLoS ONE 7(3): e32017, doi: 10.1371/journal.pone.0032017.
Szarzynska B, Sobkowiak L, Pant BD, Balazadeh S, Scheible WR, Mueller-Roeber B, Jarmolowski A, Szweykowska-Kulinska Z (2009) Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs. Nucleic Acids Res 37: 3083–3093, doi: 10.1093/nar/gkp189.
Szweykowska-Kulinska Z, Jarmolowski A, Vazquez F (2013) The crosstalk between plant microRNA biogenesis factors and the spliceosome. Plant Signal Behav 8: e26955, http://dx.doi.org/10.4161/psb.26955.
Vazquez F, Gasciolli V, Crete, P, and 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.
Wang L, Song X, Gu L, Li X, Cao S, Chu C, Cui X, Chen X, Cao X (2013) NOT2 Proteins Promote Polymerase II-Dependent Transcription and Interact with Multiple MicroRNA Biogenesis Factors in Arabidopsis. Plant Cell 25:2, 715-27, doi:10.1105/tpc.112.105882.
Xie Z, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13: 784-789.
Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis miRNA genes. Plant Physiol 138: 2145-2154.
Yan K, Liu P, Wu CA, Yang GD, Xu R, Guo QH, Huang JG, Zheng CC (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48: 521-31, http://dx.doi.org/10.1016/j.molcel.2012.08.032.
Zhan X, Wang B, Li H, Liu R, Kalia RK, Zhu JK (2012) Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proc Natl Acad Sci USA 109: 44, 18198-18203, doi:10.1073/pnas.1216199109.
Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102: 509-519, doi: 10.1093/aob/mcn129.
Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101(3): 187-94, http://dx.doi.org/10.1016/j.ygeno.2012.12.004.
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 of Exp Bot 61: 4157-4168, doi: 10.1093/jxb/erq237.
Zielezinski A, Dolata J, Alaba S, Kruszka K, Pacak A, Swida-Barteczka A, Knop K, Stepien A, Bielewicz D, Pietrykowska H, Sierocka I, Sobkowiak L, Lakomiak A, Jarmolowski A, Szweykowska-Kulinska Z, Karlowski WM (2015) mirEX 2.0 – an integrated environment for expression profiling of plant microRNAs. BMC Plant Biol 15: 144, doi: 10.1186/s12870-015-0533-2.
Acta Biochimica Polonica is an open access quarterly and publishes four issues a year. All contents are distributed under the Creative Commons Attribution-ShareAlike 4.0 International (CC BY-SA 4.0) license. Everybody may use the content following terms: Attribution — You must give appropriate credit, provide a link to the license, and indicate if changes were made, ShareAlike — If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original. There are no additional restrictions — You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.
Copyright for all published papers © stays with the authors.
Copyright for the journal: © Polish Biochemical Society.