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In silico prediction of miRNAs targeting ToLCV and their regulation in susceptible and resistant tomato plants

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Abstract

Tomato leaf curl disease is one of the main constraints in tomato production worldwide. It is induced by viruses including Tomato leaf curl virus (ToLCV). Plant viruses can both induce and be themselves targeted by gene silencing machinery. Certain animal viruses were found to be targeted by host miRNAs but, there is no similar experimental report for plant viruses. In this study, we investigated if tomato-encoded miRNAs target ToLCV using an in silico analysis. Results showed that ToLCV can be targeted by three tomato miRNAs, named miR156, miR159, and miR403. Following virus infection of susceptible tomato plants cv Moneymaker, miR159 and miR403 were upregulated, while miR156 was unchanged. In the plants of the resistant tomato variety PS550, that accumulated 50-fold less viral DNA and did not show disease symptoms, miR156 was upregulated, while the two others remained unchanged. In addition, the expression level of three genes known as targets of these miRNAs, i.e. SPL6b, MYB33 and AGO2a, was measured in both susceptible and resistant tomato varieties by qRT-PCR. The possible role of the predicted miRNAs and regulation of their target genes in symptom development by ToLCV is discussed.

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References

  • Accotto G, Navas-Castillo J, Noris E, Moriones E, Louro D (2000) Typing of tomato yellow leaf curl viruses in Europe. Eur J Plant Pathol 106:179–186

    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 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Bisaro DM (1996) Geminivirus DNA replication. In: DePamphilis ML (ed) DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 833–854

    Google Scholar 

  • Brosseau C, Jaubert M, Zamora A, Moffett P (2011) Identification of an ARGONAUTE for antiviral RNA silencing in Nicotiana benthamiana. Plant Physiol 156:1548–1555

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Silva JCF, Fiallo-Olivé E, Briddon RW, Hernández-Zepeda C, Idris A, Malathi VG, Martin DP, Rivera-Bustamante R, Ueda S, Varsani A (2015) Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 160:1593–1619

    Article  CAS  PubMed  Google Scholar 

  • Butterbach P, Verlaan MG, Dullemans A, Lohuis D, Visser RGF, Bai YL et al (2014) Tomato yellow leaf curl virus resistance by Ty-1 involves increased cytosine methylation of viral genomes and is compromised by cucumber mosaic virus infection. Proc Natl Acad Sci U S A 111:12942–12947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L (2010) SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. J Integr Plant Biol 52:946–951

    Article  CAS  PubMed  Google Scholar 

  • Dry IB, Rigden JE, Krake LR, Mullineaux PM, Rezaian MA (1993) Nucleotide sequence and genome organization of tomato leaf curl geminivirus. J Gen Virol 74:147–151

    Article  CAS  PubMed  Google Scholar 

  • Dry IB, Krake LR, Rigden JE, Rezaian MA (1997) A novel subviral agent associated with a geminivirus: the first report of a DNA satellite. Proc Natl Acad Sci U S A 94:7088–7093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  CAS  PubMed  Google Scholar 

  • Friedmann M, Lapidot M, Cohen S, Pilowsky M (1998) A novel source of resistance to Tomato yellow leaf curl virus exhibiting a symptomless reaction to viral infection. J. Am Soc Hortic Sci 123:1004–1007

    Google Scholar 

  • Ghanbari M, Eini O, Ebrahimi S (2016) Differential expression of MYB33 and AP2 genes and response of TY resistant plants to Beet curly top iran virus infection in tomato. J Plant Pathol 98:555–562

    Google Scholar 

  • Harvey JJW, Lewsey MG, Patel K, Westwood J, Heimstadt S, Carr JP, Baulcombe DC (2011) An antiviral defense role of AGO2 in plants. PLoS One 6:e14639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin D, Wang Y, Zhao Y, Chen M (2013) MicroRNAs and their cross-talks in plant development. J Genet Genomics 40:161–170

    Article  CAS  PubMed  Google Scholar 

  • Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–1581

    Article  CAS  PubMed  Google Scholar 

  • Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene squamosa. Mol Gen Genet 250:7–16

  • Krüger J, Rehmsmeier M (2006) RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 34:451–454

    Article  Google Scholar 

  • Lapidot M, Friedmann M (2002) Breeding for resistance to whitefly-transmitted geminiviruses. Ann Appl Biol 140:109–127

    Article  Google Scholar 

  • Lin S, Wu H, Elena S, Chen K, Niu Q, Ye S, Chen C, Chua N (2009) Molecular evolution of a viral non-coding sequence under the selective pressure of a miRNA-mediated silencing. PLoS Pathog 5(2):e1000312

    Article  PubMed  PubMed Central  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 

  • Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569

    Article  CAS  PubMed  Google Scholar 

  • Mason G, Caciagli P, Accotto GP, Noris E (2008) Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci. Virol Methods 147:282–289

    Article  CAS  Google Scholar 

  • Meyers BC, Axtellb MJ, Bartelc B, Barteld DP, Baulcombee D, Bowmanf JL et al (2008) Criteria for annotation of plant microRNAs. Plant Cell 20:3186–3190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miozzi L, Napoli C, Sardo L, Accotto GP (2014) Transcriptomics of the interaction between the monopartite phloem-limited geminivirus Tomato yellow leaf curl sardinia virus and Solanum lycopersicum highlights a role for plant hormones, autophagy and plant immune system fine tuning during infection. PLoS One 9:e89951

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriones E, Navas-Castillo J (2000) Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 71:123–134

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naqvi A, Haq Q, Mukherjee S (2010) MicroRNA profiling of Tomato leaf curl new delhi virus (ToLCNDV) infected tomato leaves indicates that deregulation of miR159/319 and miR172 might be linked with leaf curl disease. Virol J 7:281

    Article  PubMed  PubMed Central  Google Scholar 

  • Naqvi AR, Choudhury NR, Mukherjee SK, Haq QMR (2011) In silico analysis reveals that several tomato microRNA/microRNA* sequences exhibit propensity to bind to Tomato leaf curl virus (ToLCV) associated genomes and most of their encoded open reading frames (ORFs). Plant Physiol Biochem 49:13–17

    Article  CAS  PubMed  Google Scholar 

  • Nath P, Sane VA, Sane AP, Trivedi PK (2006) Plant gene expression, regulation of. Rev Cell Biol Mol Med. doi:10.1002/3527600906.mcb.200400154

  • Niu Q, Lin S, Reyes J, Chen K, Wu H, Ye S, Chua N (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotech 24:1420–1427

    Article  CAS  Google Scholar 

  • Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis MicroRNAs miR159 and miR319. Dev Cell 13:115–125

    Article  CAS  PubMed  Google Scholar 

  • Perez-Quintero A, Neme R, Zapata A, Lopez C (2010) Plant microRNAs and their role in defense against viruses: a bioinformatics approach. BMC Plant Biol 10:138–150

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips J, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    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 

  • Rasmussen R (2001) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR, methods and applications. Springer Press, Heidelberg, pp 21–34

  • Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E et al (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954

    Article  CAS  PubMed  Google Scholar 

  • Seemanpillai M, Dry I, Randles J, Rezaian A (2003) Transcriptional Silencing of Geminiviral Promoter-Driven Transgenes Following Homologous Virus Infection. Molecular Plant-Microbe Interactions 16 (5):429–438

  • Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. BioTechniques 39:519–525

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1371/journal.pgen.1001031

    Article  PubMed  PubMed Central  Google Scholar 

  • Valiollahi E, Farsi M, Fevereiro P, Kakhki AM (2014) Bioinformatic characterization and expression analysis of miRNAs in Solanum lycopersicum. Plant Omics 7:108–116

    CAS  Google Scholar 

  • Van Vu T, Roy Choudhury N, Mukherjee SK (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:35–45

    Article  CAS  PubMed  Google Scholar 

  • Xia Z, Zhao Z, Chen L, Li M, Zhou T, Deng C, Zhou Q, Fan Z (2016) Synergistic infection of two viruses MCMV and SCMV increases the accumulations of both MCMV and MCMV-derived siRNAs in maize. Sci Rep 6:20520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zou Z, Zhang J, Zhang Y, Han Q, Hu T, Xu X, Liu H, Li H, Ye Z (2011) Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Behjatnia (University of Shiraz) for his scientific. This work was supported by the University of Zanjan, Iran and the Institute for Sustainable Plant Protection, National Research Council of Italy (IPSP-CNR).

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Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

    N. Tousi & Omid Eini

  2. Seed and Plant Improvement Institute (SPII), Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

    R. Ahmadvand

  3. Institute for Sustainable Plant Protection, National Research Council of Italy (IPSP-CNR), Torino, Italy

    A. Carra, L. Miozzi, E. Noris & G. P. Accotto

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  1. N. Tousi
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  2. Omid Eini
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  7. G. P. Accotto
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Correspondence to Omid Eini.

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Tousi, N., Eini, O., Ahmadvand, R. et al. In silico prediction of miRNAs targeting ToLCV and their regulation in susceptible and resistant tomato plants. Australasian Plant Pathol. 46, 379–386 (2017). https://doi.org/10.1007/s13313-017-0500-5

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  • DOI: https://doi.org/10.1007/s13313-017-0500-5

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