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Dimeric artificial microRNAs mediate high resistance to RSV and RBSDV in transgenic rice plants

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Abstract

Infection of rice with Rice stripe virus (RSV) and Rice black streaked dwarf virus (RBSDV) causes a significant loss of grain production. Due to the lack of natural resistance resources against these viruses, it is imperative to discover a biotechnological approach that will provide effective and safe immunity to RSV and RBSDV. In this study, we constructed three dimeric artificial microRNA (amiRNA) precursor expression vectors (pamiR-M, pamiR-3 and pamiR-U) that simultaneously target the CP genes of RSV and RBSDV based on the structure of the rice (Oryza sativa L.) osa-MIR528 precursor. The transgenic plants were obtained by Agrobacterium tumefaciens-mediated transformation and were shown to express amiRNAs successfully. Viral challenge assays revealed that these transgenic plants demonstrated different resistance (26.66–54.17 %) against RSV and RBSDV infection simultaneously. The amiRNA-targeting 3′-UTR region of CP gene (pamiR-U) induced higher virus resistance: 54.17 % against RSV and 45.83 % against RBSDV. A northern blot assay indicated that there was a good correlation between the resistance level and amiRNAs accumulation. The RNA silencing induced by the original amiRNAs could be bilaterally extended by the siRNA pathway. The amiRNAs, together with the secondary siRNAs, mediated the degradation of viral RNAs. A genetic stability assay showed that transgenes and amiRNA-mediated virus resistance could be stably inherited in the transgenic plants.

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References

  • Ai T, Zhang L, Gao Z, Zhu CX, Guo X (2011) Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol 3:304–316

    Article  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  CAS  PubMed  Google Scholar 

  • Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azuhata F, Uyeda I, Shikata E (1992) Conserved terminal nucleotide sequences in the genome of Rice black streaked dwarf virus. J Gen Virol 73:1593–1595

    Article  CAS  PubMed  Google Scholar 

  • Azzam O, Chancellor TCB (2002) The biology, epidemiology, and Management of rice tungro disease in Asia. Plant Dis 86:88–100

    Article  CAS  Google Scholar 

  • Bai FW, Qu ZC, Yan J, Zhang HW, Xu J, Ye MM, Wu HL, Liao XG, Shen DL (2001) Identification of Rice black streaked dwarf virus in different cereal crops with dwarfing symptoms in China. Acta Virol 45:335–339

    CAS  PubMed  Google Scholar 

  • Barbier P, Takahashi M, Nakamura I, Toriyama S, Ishihama A (1992) Solubilization and promoter analysis of RNA polymerase from rice stripe virus. J Virol 66:6171–6174

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe D (2005) RNA silencing. Trends Biochem Sci 30:290–293

    Article  CAS  PubMed  Google Scholar 

  • Braunstein TH, Moury B, Johannessen M, Albrechtsen M (2002) Specific degradation of 3′ regions of GUS mRNA in posttranscriptionally silenced tobacco lines may be related to 5′–3′ spreading of silencing. RNA 8:1034–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bucher E, Sijen T, De Haan P, Goldbach R, Prins M (2003) Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J Virol 77:1329–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castanotto D, Rossi JJ (2009) The promises and pitfalls of RNA-interference-based therapeutics. Nature 457:426–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan CY, Carmack CS, Long DD, Maliyekkel A, Shao Y, Roninson IB, Ding Y (2009) A structural interpretation of the effect of GC-content on efficiency of RNA interference. BMC Bioinform 10(Suppl 1):S33

    Article  Google Scholar 

  • Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol 150:1111–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps. Nature 460:479–486

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho WK, Lian S, Kim SM, Park SH, Kim KH (2013) Current insights into research on Rice stripe virus. Plant Pathol J 29:223–233

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui GR, Wu H, Liu YG (2004) Selecting herbicide-resistant calli of rice and appraising to seedling with PPT and Basta. Seed 23:7–10

    Google Scholar 

  • Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan CG, Wang CH, Fang RX, Guo HS (2008) Artificial MicroRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol 82:11084–11095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835–840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa T, Zhu Y, Itoh K, Kimura Y, Izawa T, Shimamoto K, Toriyama S (1992) Genetically engineered rice resistant to Rice stripe virus, an insect transmitted virus. PANS 89:9865–9869

    Article  CAS  Google Scholar 

  • Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H (2002) Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucleic Acids Res 30:1757–1766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12:99–110

    Article  CAS  PubMed  Google Scholar 

  • Ishikama K, Omura T, Hibino H (1989) Morphological characteristics of Rice stripe virus. J Gen Virol 70:3465–3468

    Article  Google Scholar 

  • Isogai M, Uyeda I, Lee BC (1998) Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. J Gen Virol 79:1487–1494

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Song YZ, Han QJ, Zhu CX, Wen FJ (2011a) The choice of target site is crucial in artificial miRNA-mediated virus resistance in transgenic Nicotiana tabacum. Physiol Mol Plant Pathol 76:2–8

    Article  CAS  Google Scholar 

  • Jiang F, Wu B, Zhang C, Song Y, An H, Zhu C, Wen F (2011b) Special origin of stem sequence influence the resistance of hairpin expressing plants against PVY. Biol Plant 55:528–535

    Article  CAS  Google Scholar 

  • Jiang Y, Sun L, Jiang M, Li K, Song Y, Zhu C (2013) Production of marker-free and RSV-resistant transgenic rice using a twin T-DNA system and RNAi. J Biosci 38:573–581

    Article  CAS  PubMed  Google Scholar 

  • Kakutani T, Hayano Y, Hayashi T, Minobe Y (1990) Ambisense segment 4 of Rice stripe virus: possible evolutionary relationship with phleboviruses and uukuviruses (Bunyaviridae). J Gen Virol 71:1427–1432

    Article  CAS  PubMed  Google Scholar 

  • Kakutani T, Hayano Y, Hayashi T, Minobe Y (1991) Ambisense segment 3 of Rice stripe virus: the first instance of a virus containing two ambisense segments. J Gen Virol 72:465–468

    Article  CAS  PubMed  Google Scholar 

  • Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385

    Article  CAS  PubMed  Google Scholar 

  • Kung YJ, Lin SS, Huang YL, Chen TC, Harish SS, Chua NH, Yeh SD (2012) Multiple artificial microRNAs targeting conserved motifs of the replicase gene confer robust transgenic resistance to negative-sense single-stranded RNA plant virus. Mol Plant Pathol 13:303–317

    Article  CAS  PubMed  Google Scholar 

  • Le WJ (2010) Transient expression of RSV gene in the Nicotiana benthamiana and the relationship between immune-related gene expression level in Laodelphax striatellus and RSV infection. Nanjing Normal University. doi:10.7666/d.y1726606

  • Li HW (2011) Production of markergene-free transgenic rice resistant to RSV and RBSDV mediated by RNA interference. Chinese Academy of Agricultural Sciences

  • Li J, Andika IB, Shen J, Lv Y, Ji Y, Sun L, Chen J (2013) Characterization of rice black-streaked dwarf virus- and Rice stripe virus-derived siRNAs in singly and doubly infected insect vector Laodelphax striatellus. PLoS ONE 8:e66007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XC, Pan CX, Song YZ, Chen HL, Wen FJ (1995) A simple procedure of DNA isolation from monocotyledonous plants and its application. J Shandong Agric Univ (Natural science) 26:491–495

    Google Scholar 

  • Liu ZZ, Wang JL, Huang X, Xu WH, Liu ZM, Fang RX (2003) The promoter of a rice glycine-rich protein gene, Osgrp-2, confers vascular-specific expression in transgenic plants. Planta 216:824–833

    CAS  PubMed  Google Scholar 

  • Liu H, Wei C, Zhong Y, Li Y (2007) Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution. Virus Res 127:34–42

    Article  CAS  PubMed  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  PubMed  Google Scholar 

  • Luo KQ, Chang DC (2004) The gene-silencing efficiency of siRNA is strongly dependent on the local structure of mRNA at the targeted region. Biochem Biophys Res Commun 318:303–310. doi: 10.1007/s11248-011-9502-1. Epub 2011 May 1

  • Ma J, Song Y, Wu B, Jiang M, Li K, Zhu C, Wen F (2011) Production of transgenic rice new germplasm with strong resistance against two isolations of Rice stripe virus by RNA interference. Transgenic Res 20:1367–1377

    Article  CAS  PubMed  Google Scholar 

  • Martínez F, Elena SF, Daròs JA (2013) Fate of artificial microRNA-mediated resistance to plant viruses in mixed infections. Phytopathology 103:870–876

    Article  PubMed  Google Scholar 

  • Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15:185–197

    Article  CAS  PubMed  Google Scholar 

  • Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, Lim B, Rigoutsos I (2006) A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126:1203–1217

    Article  CAS  PubMed  Google Scholar 

  • Muthayya S, Sugimoto JD, Montgomery S, Maberly GF (2014) An overview of global rice production, supply, trade, and consumption. Ann NY Acad Sci 1324:7–14

    Article  PubMed  Google Scholar 

  • Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • Noda S, Omura T, Murakami M, Tsuchizaki T (1991) Infectivity of rice Viruses to the varieties resistant to Rice stripe virus. Ann Phytopathol Soc Jpn 57:259–262

    Article  Google Scholar 

  • Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–2242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasquinelli AE (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13:271–282

    CAS  PubMed  Google Scholar 

  • Patzel V, Rutz S, Dietrich I, Köberle C, Scheffold A, Kaufmann SH (2005) Design of siRNAs producing unstructured guide-RNAs results in improved RNA interference efficiency. Nat Biotechnol 23:1440–1444

    Article  CAS  PubMed  Google Scholar 

  • Qu Z, Liang D, Harper G, Hull R (1997) Comparison of sequences of RNAs 3 and 4 of Rice stripe virus from China with those of Japanese isolates. Virus Genes 15:99–103

    Article  CAS  PubMed  Google Scholar 

  • Qu J, Ye J, Fang R (2007) Artificial microRNA-mediated virus resistance in plants. J Virol 81:6690–6699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanford JC, Johnson SA (1985) The concept of parasite-derived resistance: deriving resistance genes from the parasite own genome. J Theor Biol 113:395–405

    Article  Google Scholar 

  • Schubert S, Grünweller A, Erdmann VA, Kurreck J (2005) Local RNA target structure influences siRNA efficacy: systematic analysis of intentionally designed binding regions. J Mol Biol 348:883–893

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Nakazono-Nagaoka E, Akita F, Uehara-Ichiki T, Omura T, Sasaya T (2011a) Immunity to Rice black streaked dwarf virus, a plant reovirus, can be achieved in rice plants by RNA silencing against the gene for the viroplasm component protein. Virus Res 160:400–403

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T, Nakazono-Nagaoka E, Uehara-Ichiki T, Sasaya T, Omura T (2011b) Targeting specific genes for RNA interference is crucial to the development of strong resistance to Rice stripe virus. Plant Biotechnol J 9:503–512

    Article  CAS  PubMed  Google Scholar 

  • Simón-Mateo C, García JA (2006) MicroRNA-guided processing impairs Plum pox virus replication, but the virus readily evolves to escape this silencing mechanism. J Virol 80:2429–2436

    Article  PubMed  PubMed Central  Google Scholar 

  • Simón-Mateo C, García JA (2011) Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta 1809:722–731

    Article  PubMed  Google Scholar 

  • Siomi MC, Sato K, Pezic D, Aravin AA (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12:246–258

    Article  CAS  PubMed  Google Scholar 

  • Song YZ, Han QJ, Jiang F, Sun RZ, Fan ZH, Zhu CX, Wen FJ (2014) Effects of the sequence characteristics of miRNAs on multi-viral resistance mediated by single amiRNAs in transgenic tobacco. Plant Physiol Biochem 77:90–98

    Article  CAS  PubMed  Google Scholar 

  • Sun RH, Du P, Jiang L, An DR, Li Y (2014) Heterologous expression of artificial miRNAs from rice dwarf virus in transgenic rice. Plant Cell Tiss Organ Cult 116:353–360

    Article  CAS  Google Scholar 

  • Takahashi M, Toriyama S, Kikuchi Y, Hayakawa T, Ishihama A (1990) Complementarity between the 5′- and 3′-terminal sequences of Rice stripe virus RNAs. J Gen Virol 71:2817–2821

    Article  CAS  PubMed  Google Scholar 

  • Takahashi M, Toriyama S, Hamamatsu C, Ishihama A (1993) Nucleotide sequence and possible ambisense coding strategy of Rice stripe virus RNA segment 2. J Gen Virol 74:769–773

    Article  CAS  PubMed  Google Scholar 

  • Tiwari M, Sharma D, Trivedi PK (2014) Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Mol Biol 86:1–18

    Article  CAS  PubMed  Google Scholar 

  • Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  CAS  PubMed  Google Scholar 

  • Wang ZH, Fang SG, Xu JL, Sun LY, Li DW, Yu JL (2003) Sequence analysis of the complete genome of rice black-streaked dwarf virus isolated from maize with rough dwarf disease. Virus Genes 27:163–168

    Article  PubMed  Google Scholar 

  • Wang GZ, Zhou YJ, Chen ZX, Zhou XP (2004) Production of monoclonal antibodies to Rice stripe virus and application in virus detection. Acta Phytophylacica Sinica 34:302–306

    CAS  Google Scholar 

  • Wang XQ, Shen X, He YM, Ren TN, Wu WT, Xi T (2011) An optimized freeze-thaw method for transformation of Agrobacterium tumefaciens EHA105 and LBA4404. Pharm Biotechnol 18:382–386

    CAS  Google Scholar 

  • Warthmann N, Chen H, Ossowski S, Weigel D, Hervé P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3:e1829

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu JX, Ni YQ, Liu H, Rao LX, Zhou YJ (2013) Development and use of three monoclonal antibodies for the detection of rice black-streaked dwarf virus in field plants and planthopper vectors. Virol J 10:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong R, Wu J, Zhou Y, Zhou X (2009) Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387:29–40

    Article  CAS  PubMed  Google Scholar 

  • Yan XT, Wang JF, Qiu BS, Tian P (1997) Resistance to Rice stripe virus conferred by expression of coat protein in transgenic indica rice plants regenerated from bombarded suspension culture. Virol Sin 12:260–269

    Google Scholar 

  • Yan F, Lu Y, Wu G, Peng J, Zheng H, Lin L, Chen J (2012) A simplified method for constructing artificial microRNAs based on the osa-MIR528 precursor. J Biotechnol 160:146–150

    Article  CAS  PubMed  Google Scholar 

  • Zhang HM, Chen JP, Adams MJ (2001) Molecular characterisation of segments 1 to 6 of Rice black-streaked dwarf virus from China provides the complete genome. Arch Virol 146:2331–2339

    Article  CAS  PubMed  Google Scholar 

  • Zhang XH, Li HX, Zhang JH, Zhang CJ, Gong PJ, Ziaf K, Xiao FM, Ye ZB (2011a) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res 20:569–581

    Article  CAS  PubMed  Google Scholar 

  • Zhang YX, Wang Q, Jiang L, Liu LL, Wang BX, Shen YY, Cheng XN, Wan JM (2011b) Fine mapping of qSTV11(KAS), amajor QTL for rice stripe disease resistance. Theor Appl Genet 122:1591–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Xie XY, Song YZ, Jiang F, Zhu CX, Wen FJ (2013) Viral resistance mediated by shRNA depends on the sequence similarity and mismatched sites between the target sequence and siRNA. Biol Plant 57:547–554

    Article  CAS  Google Scholar 

  • Zhou T, Zhou YJ, Cheng ZB, Yang RM, Ji J (2007) Identification of resistance to Rice stripe virus in japonica rice varieties and analysis for its inheritance of Zhendao 88. Acta Phytophylacica Sinica 35:475–479

    Google Scholar 

  • Zhou T, Wu LJ, Wang Y, Cheng ZB, Ji Yh, Fan YJ, Zhou YJ (2011) Transmission of Rice black–streaked dwarf virus from frozen infected leaves to healthy rice plants by small brown planthopper (Laodelphax striatellus). Rice Sci 18:152–156

    Article  Google Scholar 

  • Zhou T, Du L, Wang L, Wang Y, Gao C, Lan Y, Sun F, Fan Y, Wang G, Zhou Y (2015) Genetic analysis and molecular mapping of QTLs for resistance to rice black-streaked dwarf disease in rice. Sci Rep 5:10509

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Hayakawa T, Toriyama S, Takahashi M (1991) Complete nucleotide sequence of RNA 3 of Rice stripe virus: an ambisense coding strategy. J Gen Virol 72:763–767

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Hayakawa T, Toriyama S (1992) Complete nucleotide sequence of RNA 4 of Rice stripe virus isolate T, and comparison with another isolate and with maize stripe virus. J Gen Virol 73:1309–1312

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported in part by the China National Transgenic Plant Research and Commercialization Project (Grant No. 2014ZX08001-002).

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    1. State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China

      Lin Sun, Chao Lin, Jinwen Du, Yunzhi Song, Hongmei Liu, Shumei Zhou, Fujiang Wen & Changxiang Zhu

    2. Rice Science Research Institute, Shandong Academy of Agricultural Science, Jinan, 250100, People’s Republic of China

      Mingsong Jiang

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    Correspondence to Fujiang Wen or Changxiang Zhu.

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    Lin Sun and Chao Lin have contributed equally to this work.

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    Sun, L., Lin, C., Du, J. et al. Dimeric artificial microRNAs mediate high resistance to RSV and RBSDV in transgenic rice plants. Plant Cell Tiss Organ Cult 126, 127–139 (2016). https://doi.org/10.1007/s11240-016-0983-8

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