Abstract
Plant cell cultures are of particular interest in industrial applications as a source of biologically active substances. It is difficult, however, to achieve stable production of secondary metabolites for many plant cell cultures using classical techniques. Novel approaches should be developed for removal of the inhibitor blocks that prevent pathway activation and shift the regulatory balance to the activation of entire biosynthetic pathways. MicroRNAs (miRNAs) are small RNAs that play important regulatory roles in various biological processes. Only recently miRNAs have been demonstrated as active in secondary metabolism regulation. In this work, we summarize recent data on the emerging approaches based on regulation of secondary metabolism by miRNAs.
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References
Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363
Boke H, Ozhuner E, Turktas M, Parmaksiz I, Ozcan S, Unver T (2015) Regulation of the alkaloid biosynthesis by miRNA in opium poppy. Plant Biotechnol J. doi:10.1111/pbi.12346
Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503
Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Vereshchagina YV (2013) Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotechnol 134:1–22
Bulgakov VP, Veremeichik GN, Shkryl YN (2015) The rolB gene activates the expression of genes encoding microRNA processing machinery. Biotechnol Lett 37:921–925
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037
Georgiev MI, Weber J (2014) Bioreactors for plant cells: hardware configuration and internal environment optimization as tools for wider commercialization. Biotechnol Lett 36:1359–1367
Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522
Hao DC, Yang L, Xiao PG, Liu M (2012) Identification of Taxus microRNAs and their targets with high-throughput sequencing and degradome analysis. Physiol Plant 146:388–403
He X, Sun Q, Jiang H, Zhu X, Mo J, Long L, Xiang L, Xie Y, Shi Y, Yuan Y, Cai Y (2014) Identification of novel microRNAs in the Verticillium wilt-resistant upland cotton variety KV-1 by high-throughput sequencing. Springerplus 3:564
Kettles GJ, Drurey C, Schoonbeek HJ, Maule AJ, Hogenhout SA (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198:1178–1190
Khojasteh A, Mirjalili MH, Hidalgo D, Corchete P, Palazon J (2014) New trends in biotechnological production of rosmarinic acid. Biotechnol Lett 36:2393–2406
Laubinger S, Zeller G, Henz SR, Buechel S, Sachsenberg T, Wang JW, Rätsch 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
Legrand S, Valot N, Nicolé F, Moja S, Baudino S, Jullien F, Magnard JL, Caissard JC, Legendre L (2010) One-step identification of conserved miRNAs, their targets, potential transcription factors and effector genes of complete secondary metabolism pathways after 454 pyrosequencing of calyx cDNAs from the Labiate Salvia sclarea L. Gene 450:55–62
Li S, Zachgo S (2013) TCP3 interacts with R2R3-MYB proteins, promotes flavonoid biosynthesis and negatively regulates the auxin response in Arabidopsis thaliana. Plant J 76:901–913
Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou JM (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152:2222–2231
Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun YH, Yuan L, Yeh TF, Peszlen I, Ralph J, Sederoff RR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110:10848–10853
Luo QJ, Mittal A, Jia F, Rock CD (2012) An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis. Plant Mol Biol 80:117–129
Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439
Ng DW, Zhang C, Miller M, Palmer G, Whiteley M, Tholl D, Chen ZJ (2011) cis- and trans-regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 23:1729–1740
Niemeier S, Junior LA, Merkle T (2010) Improvement of the design and generation of highly specific plant knockdown lines using primary synthetic microRNAs (pri-smiRNAs). BMC Res Notes 3:59
Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690
Pani A, Mahapatra RK (2013) Computational identification of microRNAs and their targets in Catharanthus roseus expressed sequence tags. Genomics Data 1:2–6
Ren G, Yu B (2012) Critical roles of RNA-binding proteins in miRNA biogenesis in Arabidopsis. RNA Biol 9:1424–1428
Robert-Seilaniantz A, MacLean D, Jikumaru Y, Hill L, Yamaguchi S, Kamiya Y, Jones JD (2011) The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J 67:218–231
Ronemus M, Vaughn MW, Martienssen RA (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–1574
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527
Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133
Tang M, Mao D, Xu L, Li D, Song S, Chen C (2014) Integrated analysis of miRNA and mRNA expression profiles in response to Cd exposure in rice seedlings. BMC Genom 15:835
Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6:e1001031
Trumbo JL, Zhang B, Stewart CN Jr (2015) Manipulating microRNAs for improved biomass and biofuels from plant feedstocks. Plant Biotechnol J 13:337–354
Tuteja JH, Zabala G, Varala K, Hudson M, Vodkin LO (2009) Endogenous, tissue-specific short interfering RNAs silence the chalcone synthase gene family in Glycine max seed coats. Plant Cell 21:3063–3077
Vashisht I, Mishra P, Pal T, Chanumolu S, Singh TR, Chauhan RS (2015) Mining NGS transcriptomes for miRNAs and dissecting their role in regulating growth, development, and secondary metabolites production in different organs of a medicinal herb Picrorhiza kurroa. Planta. doi:10.1007/s00425-015-2255-y
Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243
Wang M, Soyano T, Machida S, Yang JY, Jung C, Chua NH, Yuan YA (2011) Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev 25:64–76
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 25:715–727
Xia R, Zhu H, An YQ, Beers EP, Liu Z (2012) Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol 13:R47
Yu ZX, Wang LJ, Zhao B, Shan CM, Zhang YH, Chen DF, Chen XY (2015) Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and Patchouli (Pogostemon cablin) by the miR156-targeted SPL transcription factors. Mol Plant 8:98–110
Zhang W, Gao S, Zhou X, Chellappan P, Chen Z, Zhou X, Zhang X, Fromuth N, Coutino G, Coffey M et al (2011) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 75:93–105
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This work was supported by a Grant from the Russian Science Foundation (Grant Number 14-14-00230).
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Bulgakov, V.P., Avramenko, T.V. New opportunities for the regulation of secondary metabolism in plants: focus on microRNAs. Biotechnol Lett 37, 1719–1727 (2015). https://doi.org/10.1007/s10529-015-1863-8
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DOI: https://doi.org/10.1007/s10529-015-1863-8