Abstract
MicroRNAs (miRNAs) are a class of small endogenous non-coding RNAs that modulate gene expression in both plants and animals and are involved in several biological processes, ranging from organ differentiation to biotic and abiotic stress responses. We identified two cold stress response microRNAs that showed differential expression in Solanum lycopersicum plants subjected to cold stress. We observed that Sly-miR166 and Sly-miR319 were up-regulated by cold treatments. The up-regulation of Sly-miR166 and Sly-miR319 in cold stress-treated S. lycopersicum seedlings and the down-regulation of their respective targets, HD-Zip III and GAMyb-like that validate by 5′-RACE technique, suggests that these miRNAs play a critical role in regulating S. lycopersicum responses to cold stress.
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References
Addo-Quaye C, Miller W, Axtell MJ (2009) Cleave Land: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25(1):130–131
Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645
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
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought-and ABA-regulated gene expression. Plant Mol Biol 24:701–713
Bartel D (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281–297
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233
Benedict C, Geisler M, Trygg J, Huner N, Hurry V (2006) Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol 141:1219–1232
Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030
Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887
Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931
Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH (2005) Real-time quantification of microRNAs by stem–loop RT-PCR. Nucleic Acids Res 33:179–188
Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:155–159
Ding D, Zang L, Wang H, Liu Z, Zang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J 33:751–763
Eamens AL, Agius C, Smith NA, Waterhouse PM, Wang MB (2011) Efficient silencing of endogenous microRNAs using artificial microRNAs in Arabidopsis thaliana. Mol Plant 4:157–170
Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693
Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132
Hawker NP, Bowman JL (2004) Roles for class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–2270
Hwang EW, Kim KA, Park SC, Jeong MJ, Byun MO, Kwon HB (2005) Expression profiles of hot pepper (Capsicum annum) genes under cold stress conditions. J Biosci 30(5):657–667
Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153
Jian X, Zhang L, Li G, Wang X, Cao X, Fang X, Chen F (2010) Identification of novel stress-regulated microRNAs from Oryza sativa L. Genomics 95:47–55
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Karlova R, van Haarst JC, Maliepaard C, van de Geest H, Bovy AG, Lammers M, Angenent GC, de Maagd RA (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot 64(7):1863–1878
Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217
Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385
Kim VN, Nam JW (2006) Genomics of microRNA. Trends Genet 22:165–173
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
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
Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Zhou H, Qu LH, Chen YQ (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583:723–728
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
Morsy MR, Almutairi A, Gibbons J, Yun SJ, de los Reyes BG (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180
Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher RL, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609
Mundy J, Yamaguchi-Shinozaki K, Chua NH (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87:1406–1410
Navaud O, Dabos P, Carnus E, Tremousaygue D, Hervé C (2007) TCP transcription factors predate the emergence of land plants. J Mol Evol 65:23–33
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
Pedranzani H, Sierra-de-Grado R, Vigliocco A, Miersch O, Abdala G (2007) Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regul 52:111–116
Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT PCR. Nucleic Acids Res 29:e45
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Rasmussen R (2001) Quantification on the light cycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR: methods and applications. Springer, New York, pp 21–34
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520
Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6(9):e230. doi:10.1371/journal.pbio.0060230
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6(5):410–417
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309
Thiebaut F, Rojas CA, Almeida KL, Grativol C, Domiciano GC, Lamb CR, Engler Jde A, Hemerly AS, Ferreira PC (2012) Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ 35(3):502–512
Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40(15):e115
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
Vasudevan S, Tong YC, Steitz JA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318:1931–1934
Wang LJ, Li SH (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2 + homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694
Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511
Woodger FJ, Millar A, Murray F, Jacobsen JV, Gubler F (2003) The role of GAMYB transcription factors in GA-regulated gene expression. J Plant Growth Regul 22:176–184
Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the riceWRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137(1):176–189
Xie F, Frazier TP, Zhang B (2010) Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). Planta 232:417–434
Yazaki J, Shimatani Z, Hashimoto A, Nagata Y, Fujii F, Kojima K, Suzuki K, Taya T, Tonouchi M, Nelson C, Nakagawa A, Otomo Y, Murakami K, Matsubara K, Kawai J, Carninci P, Hayashizaki Y, Kikuchi S (2004) Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. Physiol Genomics 17:87–100
Zhang J, Zeng R, Chen J, Liu X, Liao Q (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7
Zhang J, Xu Y, Huan Q, Chong K (2009) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449
Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788
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Valiollahi, E., Farsi, M. & Kakhki, A.M. Sly-miR166 and Sly-miR319 are components of the cold stress response in Solanum lycopersicum . Plant Biotechnol Rep 8, 349–356 (2014). https://doi.org/10.1007/s11816-014-0326-3
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DOI: https://doi.org/10.1007/s11816-014-0326-3