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Identification and validation of sugarcane streak mosaic virus-encoded microRNAs and their targets in sugarcane

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Abstract

Key message

Identification of miRNAs encoded by sugarcane streak mosaic virus and understanding their host target genes might be used as a new strategy to study viral pathogenesis and controlling mosaic disease in sugarcane.

Abstract

Plants have developed several defense mechanisms to cope with various pathogens (bacteria, fungi, virus, and phytoplasma). Among these, RNA interference (RNAi)-mediated defense against viral infection was found to be a major innate immune response. As a counter attack strategy against the host defense, viruses produce suppressors of host RNAi pathway. MicroRNAs (miRNAs) are an abundant class of short (~18–22 nucleotide) non-coding single-stranded RNAs involved in RNAi pathway leading to post-transcriptional regulation of gene expression. Sugarcane streak mosaic virus (SCSMV) is a distinct strain of Potyviridae family which has a single-stranded positive-sense RNA genome causing mosaic disease in sugarcane. In this study, we computationally predicted and experimentally validated the miRNA encoded by the SCSMV genome with detection efficiency of 99.9 % in stem-loop RT-qPCR and predicted their potential gene targets in sugarcane. These sugarcane target genes considerably broaden future investigation of the SCSMV-encoded miRNA function during viral pathogenesis and might be applied as a new strategy for controlling mosaic disease in sugarcane.

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Abbreviations

Bp:

Base pair

DIG:

Digeoxigenin

EtBr:

Ethidium bromide

FW:

Fresh weight

GO:

Gene ontology

miRNA:

MicroRNA

RNAi:

RNA interference

RT-qPCR:

Reverse transcription-quantitative PCR

UTR:

Untranslated region

References

  • Bagyalakshmi K, Parameswari B, Chinnaraja C, Karuppaiah R, Ganesh Kumar V, Viswanathan R (2012) Genetic variability and potential recombination events in the HC-Pro gene of sugarcane streak mosaic virus. Arch Virol 157:1371–1375

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Achard LS, Schaller H, Khafif M, Schott G, Bendahmane A, Voinnet O (2011) Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis. Proc Natl Acad Sci USA 109:1778–1783

    Article  Google Scholar 

  • Canonne J, Nicolas SF, Rivas S (2011) Phospholipases in action during plant defense signaling. Plant Signal Behav 6:13–18

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao Y, Yang Y, Zhang H, Li D, Zheng Z, Song F (2008) Overexpression of a rice defense-related F-box protein gene OsDRF1 in tobacco improves disease resistance through potentiation of defense gene expression. Physiol Plant 134:440–452

    Article  CAS  PubMed  Google Scholar 

  • Cho SY, Cho WK, Sohn SH, Kim KH (2012) Interaction of the host protein NbDnaJ with Potato virus X minus-strand stem-loop 1 RNA and capsid protein affects viral replication and movement. Biochem Biophys Res Comm 417:451–456

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J System Bioinfor 4:343–362

    Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucl Acids Res W155–159

  • Dai X, Zhuang Z, Zhao PX (2011) Computational analysis of miRNA targets in plants: current status and challenges. Brief Bioinform 12:115–121

    Article  CAS  PubMed  Google Scholar 

  • Espinoza C, Medina C, Somerville S, Arce-Johnson P (2007) Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. J Exp Bot 58:3197–3212

    Article  CAS  PubMed  Google Scholar 

  • Forman JJ, Miller AL, Coller HA (2008) A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci USA 105:14879–14884

    Article  CAS  PubMed  Google Scholar 

  • Gao R, Liu P, Wong SM (2012) Identification of a plant viral RNA genome in the nucleus. PLoS ONE 7:e48736

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gasic EV, 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

    Article  Google Scholar 

  • Grundhoff A (2011) Computational prediction of viral miRNAs. Methods Mol Biol 721:143–152

    Article  CAS  PubMed  Google Scholar 

  • Hofius D, Maier AT, Dietrich C, Jungkunz I, Bornke F, Maiss E, Sonnewald U (2007) Capsid protein-mediated recruitment of host DnaJ-like proteins is required for potato virus Y infection in tobacco plants. J Virol 81:11870–11880

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang P, Wu H, Wang W, Ma W, Sun X, Lu Z (2007) MiPred: classification of real and pseudo microRNA precursors using random forest prediction model with combined features. Nucl Acids Res 35:339–344

    Article  Google Scholar 

  • Kumar S, Ansari FA, Scaria V (2009) Prediction of viral microRNA precursors based on human microRNA precursor sequence and structural features. Virol J 6:129

    Article  PubMed Central  PubMed  Google Scholar 

  • Li W, He Z, Li S, Huang Y, Zhang Z, Jiang D, Wang X, Luo Z (2011) Molecular characterization of a new strain of sugarcane streak mosaic virus (SCSMV). Arch Virol 156:2101–2104

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaller HK (1987) Chlorophylls and carotenoids, pigments of photosynthetic biomembranes. Methods Enzy 148:350–382

    Article  Google Scholar 

  • Lu L, Du Z, Qin M, Wang P, Lan H, Niu X, Jia D, Xie L, Lin Q, Xie L, Wu Z (2009) Pc4, a putative movement protein of Rice stripe virus, interacts with a type I DnaJ protein and a small Hsp of rice. Virus Genes 38:320–327

    Article  CAS  PubMed  Google Scholar 

  • Lytle JR, Yario TA, Steitz JA (2007) Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci USA 104:9667–9672

    Article  CAS  PubMed  Google Scholar 

  • Page JE, Hause G, Raschke M, Gao W, Schmidt J, Zenk MH, Kutchan TM (2004) Functional analysis of the final steps of the 1-Deoxy-D-xylulose 5-phosphate (DXP) pathway to isoprenoids in plants using virus-induced gene silencing. Plant Physiol 134:1401–1413

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pantaleo V (2011) Plant RNA silencing in viral defence. Adv Exp Med Biol 722:39–58

    Article  CAS  PubMed  Google Scholar 

  • Prabu GR, Kawar PG, Dixit GB, Theerthaprasad D (2008) First report of a phytoplasma and virus pathogens associated with sugarcane grassy shoot disease in India. Sugarcane Int 26:14–16

    Google Scholar 

  • Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28:419–427

    Article  CAS  PubMed  Google Scholar 

  • Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J, Sueda K, Burgyan J, Masuta C (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog 7:e1002021

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh J, Singh CP, Bhavani A, Nagaraju J (2010) Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virol 407:120–128

    Article  CAS  Google Scholar 

  • Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombea DC (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–1521

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soellick TR, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH (2000) The movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc Natl Acad Sci USA 97:2373–2378

    Article  CAS  PubMed  Google Scholar 

  • Song L, Gao S, Jiang W, Chen S, Liu Y, Zhou L, Huang W (2011) Silencing suppressors: viral weapons for countering host cell defenses. Protein Cell 2:273–281

    Article  CAS  PubMed  Google Scholar 

  • Szcześniak MW, Deorowicz S, Gapski J, Kaczyński Ł, Makalowska I (2012) miRNEST database: an integrative approach in microRNA search and annotation. Nucl Acids Res 40:D198–D204

    Article  PubMed  Google Scholar 

  • Tatineni S, Feng Q, Ruhui L, Jack MT, Roy F (2012) Triticum mosaic poacevirus enlists P1 rather than HC-Pro to suppress RNA silencing-mediated host defense. Virology 433:104–115

    Article  CAS  PubMed  Google Scholar 

  • Thiebaut F, Grativol C, Carnavale-Bottino M, Rojas CA, Tanurdzic M, Farinelli L, Martienssen RA, Hemerly AS, Ferreira PCG (2012) Computational identification and analysis of novel sugarcane microRNAs. BMC Genomics 13:1–14

    Article  Google Scholar 

  • Thompson JR, Tepfer M (2010) Assessment of the benefits and risks for engineered virus resistance. Adv Virus Res 76:33–56

    Article  PubMed  Google Scholar 

  • Turner M, Adhikari S, Subramanian S (2013) Optimizing stem-loop qPCR assays through multiplexed cDNA synthesis of U6 and miRNAs. Plant Signal Behav 8:e24918

    Article  PubMed  Google Scholar 

  • Viswanathan R, Karuppaiah R, Balamuralikrishnan M (2009) Identification of new variants of SCMV causing sugarcane mosaic in India and assessing their genetic diversity in relation to SCMV type strains. Virus Genes 39:375–386

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Wei B, Liu H, Li T, Rayner S (2011) MiRPara: a SVM-based software tool for prediction of most probable microRNA coding regions in genome scale sequences. BMC Bioinf 12:107

    Article  CAS  Google Scholar 

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Acknowledgments

Authors are thankful to Dr. R. Vasanthakumar, Shri. K. Murugaiah, Dr. P. Lakshmanaperumalsamy, Karpagam University, Coimbatore, Tamil Nadu, India, for their encouragement and support during the course of study. The financial support in terms of research fellowship to Mr. Viswanathan Chandran by Department of Biotechnology, Government of India, New Delhi, India (BT/PR2402/AGR/36/698/2011) is also gratefully acknowledged.

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Authors and Affiliations

  1. Plant Functional Genomics Unit, Department of Biotechnology, Karpagam University, Eachanari Post, 641021, Coimbatore, Tamil Nadu, India

    Chandran Viswanathan, Jeyaraj Anburaj & Gajjeraman Prabu

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  1. Chandran Viswanathan
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  2. Jeyaraj Anburaj
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  3. Gajjeraman Prabu
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Correspondence to Gajjeraman Prabu.

Additional information

Communicated by P. Lakshmanan.

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Predicted target genes of SCSMV-encoded miR16 (XLS 47 kb)

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Viswanathan, C., Anburaj, J. & Prabu, G. Identification and validation of sugarcane streak mosaic virus-encoded microRNAs and their targets in sugarcane. Plant Cell Rep 33, 265–276 (2014). https://doi.org/10.1007/s00299-013-1527-x

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  • DOI: https://doi.org/10.1007/s00299-013-1527-x

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