Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana

详细信息    查看全文

• 作者：Wing-Sham Lee ; Shih-Feng Fu ; Zheng Li ; Alex M. Murphy…
• 关键词：Systemic acquired resistance ; Hypersensitive response ; Virus movement ; RNAi ; Post ; transcriptional gene silencing ; Effector ; triggered immunity ; Defensive signal transduction
• 刊名：BMC Plant Biology
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：16
• 期：1
• 全文大小：2,545 KB
• 参考文献：1.Lewsey MG, Palukaitis P, Carr JP. Plant-virus interactions: defence and counter-defence. In: Parker J, editor. Annual plant reviews volume 34: molecular aspects of plant disease resistance. Oxford: Blackwell; 2009. p. 134–76.
  2.Carr JP, Lewsey MG, Palukaitis P. Signaling in induced resistance. Adv Virus Res. 2010;76:57–121.PubMed CrossRef
  3.Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, et al. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet. 2000;26:403–10.PubMed CrossRef
  4.Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, Macaulay K, et al. Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant-Microbe Interact. 2010;23:835–45.PubMed CrossRef
  5.Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol. 2004;42:185–209.PubMed CrossRef
  6.Carr JP, Beachy RN, Klessig DF. Are the PR1 proteins of tobacco involved in genetically engineered resistance to TMV? Virology. 1989;169:470–3.PubMed CrossRef
  7.Cutt JR, Harpster MH, Dixon DC, Carr JP, Dunsmuir P, Klessig DF. Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related protein PR1b. Virology. 1989;173:89–97.PubMed CrossRef
  8.Linthorst HJM, Meuwissen RLJ, Kauffmann S, Bol JF. Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus-infection. Plant Cell. 1989;1:285–91.PubMed PubMedCentral CrossRef
  9.Palukaitis P, Groen SC, Carr JP. The Rumsfeld paradox: some of the things we know that we don’t know about plant virus infection. Curr Opin Plant Biol. 2013;16:513–9.PubMed CrossRef
  10.Kachroo P, Yoshioka K, Shah J, Dooner HK, Klessig DF. Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell. 2000;12:677–90.PubMed PubMedCentral CrossRef
  11.Wong CE, Carson RA, Carr JP. Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. Mol Plant-Microbe Interact. 2002;15:75–81.PubMed CrossRef
  12.Goto K, Kobori T, Kosaka Y, Natsuaki T, Masuta C. Characterisation of silencing suppressor 2b of Cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol. 2007;48:1050–60.PubMed CrossRef
  13.Gonzalez I, Martinez L, Rakitina DV, Lewsey MG, Atencio FA, Llave C, et al. Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant-Microbe Interact. 2010;23:294–303.PubMed CrossRef
  14.Gonzalez I, Rakitina D, Semashko M, Taliansky M, Praveen S, Palukaitis P, et al. RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA. 2012;18:771–82.PubMed PubMedCentral CrossRef
  15.Ji LH, Ding SW. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant-Microbe Interact. 2001;14:715–24.PubMed CrossRef
  16.Alamillo JM, Saénz P, García JA. Salicylic acid mediated and RNA-silencing defence mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. Plant J. 2006;48:217–27.PubMed CrossRef
  17.Jovel J, Walker M, Sanfaçon H. Salicylic acid-dependent restriction of Tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance. Mol Plant-Microbe Interact. 2011;24:706–18.PubMed CrossRef
  18.Xie Z, Fan B, Chen C, Chen Z. An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci U S A. 2001;98:6516–21.PubMed PubMedCentral CrossRef
  19.Yu D, Fan B, MacFarlane SA, Chen Z. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defence. Mol Plant-Microbe Interact. 2003;16:206–16.PubMed CrossRef
  20.Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Vazquez F, et al. Four plant dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 2006;34:6233–46.PubMed PubMedCentral CrossRef
  21.Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, et al. Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell. 2010;22:481–96.PubMed PubMedCentral CrossRef
  22.Fusaro AF, Matthew L, Smith NA, Curtin CJ, Dedic-Hagen J, Ellacott GA, et al. RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 2006;2006(7):1168–75.CrossRef
  23.Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, et al. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell. 2002;14:629–39.PubMed PubMedCentral CrossRef
  24.Iwakawa HO, Tomari Y. Molecular insights into microRNA-mediated translational repression in plants. Mol Cell. 2013;52:591–601.PubMed CrossRef
  25.Wassenegger M, Krczal G. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 2006;11:142–51.PubMed CrossRef
  26.Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel J-B, et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell. 2000;101:533–42.PubMed CrossRef
  27.Dalmay TD, Horsefield R, Braunstein TH, Baulcombe DC. SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 2001;20:2069–78.PubMed PubMedCentral CrossRef
  28.Schwach F, Vaistij FE, Jones L, Baulcombe DC. An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol. 2005;138:1842–52.PubMed PubMedCentral CrossRef
  29.Rakhshandehroo F, Takeshita M, Squires J, Palukaitis P. The influence of RNA-dependent RNA polymerase 1 on Potato virus Y infection and on other antiviral response genes. Mol Plant-Microbe Interact. 2009;10:1312–8.CrossRef
  30.Qin C, Shi N, Gu M, Zhang H, Li B, Shen J, et al. Involvement of RDR6 in short-range intercellular RNA silencing in Nicotiana benthamiana. Sci Rep. 2012;2:467.PubMed PubMedCentral CrossRef
  31.Harvey JJW, Lewsey MG, Patel K, Westwood JH, Heimstädt S, Carr JP, et al. An antiviral defense role of AGO2 in plants. PLoS One. 2011;6, e14639.PubMed PubMedCentral CrossRef
  32.Jaubert M, Bhattacharjee S, Mello AFS, Perry KL, Moffett P. ARGONAUTE2 mediates RNA silencing antiviral defenses and Potato virus X in Arabidopsis. Plant Physiol. 2011;156:1556–64.PubMed PubMedCentral CrossRef
  33.Scholthof HB, Alvarado VY, Vega-Arreguin JC, Ciomperlik J, Odokonyero D, Brosseau C, et al. Identification of an ARGONAUTE for antiviral RNA silencing in Nicotiana benthamiana. Plant Physiol. 2011;156:1548–55.PubMed PubMedCentral CrossRef
  34.Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, et al. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell. 2012;42:356–66.CrossRef
  35.Lewsey MG, Carr JP. Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid treated plants. J Gen Virol. 2009;90:3010–4.PubMed CrossRef
  36.Gilliland A, Singh DP, Hayward JM, Moore CA, Murphy AM, York CJ, et al. Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol. 2003;132:1518–28.PubMed PubMedCentral CrossRef
  37.Lee WS, Fu SF, Verchot-Lubicz J, Carr JP. Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biol. 2011;11:41–50.PubMed PubMedCentral CrossRef
  38.Pandey SP, Baldwin IT. RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant J. 2007;50:40–53.PubMed CrossRef
  39.Hunter LJR, Westwood JH, Heath G, Macaulay K, Smith AG, MacFarlane SA, et al. Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS One. 2013;8, e66530.PubMed PubMedCentral CrossRef
  40.Liao YWK, Sun ZH, Zhou YH, Shi K, Li X, Zhang GQ, et al. The role of hydrogen peroxide and nitric oxide in the induction of plant-encoded RNA-dependent RNA polymerase 1 in the basal defense against tobacco mosaic virus. PLoS One. 2013;8, e76090.PubMed PubMedCentral CrossRef
  41.Xu T, Zhang L, Zhen J, Fan Y, Zhang C, Wang L. Expressional and regulatory characterization of Arabidopsis RNA-dependent RNA polymerase 1. Planta. 2013;237:1561–9.PubMed CrossRef
  42.Yang SJ, Carter SA, Cole AB, Cheng NH, Nelson RS. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc Natl Acad Sci U S A. 2004;101:6297–302.PubMed PubMedCentral CrossRef
  43.Wylie SJ, Zhang C, Long V, Roossinck MJ, Koh SH, Jones MGK, et al. Differential responses to virus challenge of laboratory and wild accessions of Australian species of Nicotiana, and comparative analysis of RDR1 gene sequences. PLoS One. 2015;10, e0121787.PubMed PubMedCentral CrossRef
  44.Ying X-B, Dong L, Zhu H, Duan C-G, Du Q-S, Lv D-Q, et al. RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell. 2010;22:1358–72.PubMed PubMedCentral CrossRef
  45.Shivprasad S, Pogue GP, Lewandowski DJ, Hidalgo J, Donson J, Grill LK, et al. Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. Virology. 1999;255:312–23.PubMed CrossRef
  46.Murphy AM, Gilliland A, York CJ, Hyman B, Carr JP. High-level expression of alternative oxidase protein sequences enhances the spread of viral vectors in resistant and susceptible plants. J Gen Virol. 2004;85:3777–86.PubMed CrossRef
  47.Jupin I, Chua NH. Activation of the CaMV as-1 cis-element by salicylic acid: differential DNA-binding of a factor related to TGA1a. EMBO J. 1996;15:5679–89.PubMed PubMedCentral
  48.Butterbrodt T, Thurow C, Gatz C. Chromatin immunoprecipitation analysis of the tobacco PR-1a and the truncated CaMV 35S promoter reveals differences in salicylic acid-dependent TGA factor binding and histone acetylation. Plant Mol Biol. 2006;61:665–74.PubMed CrossRef
  49.Cheng NH, Su CL, Carter SA, Nelson RS. Vascular invasion routes and systemic accumulation patterns of tobacco mosaic virus in Nicotiana benthamiana. Plant J. 2000;23:349–62.PubMed CrossRef
  50.Shirsekar G, Dai L, Hu Y, Wang X, Zeng L, Wang G-L. Role of ubiquitination in plant innate immunity and pathogen virulence. J Plant Biol. 2010;53:1–10.CrossRef
  51.Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, et al. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J. 2007;49:79–90.PubMed CrossRef
  52.Conrath U, Klessig DF, Bachmair A. Tobacco plants perturbed in the ubiquitin-dependent protein degradation system accumulate callose, salicylic acid, and pathogenesis-related protein 1. Plant Cell Rep. 1998;17:876–80.CrossRef
  53.Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell. 2009;137:860–72.PubMed PubMedCentral CrossRef
  54.Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature. 2012;486:228–32.PubMed PubMedCentral
  55.Bailey M, Srivastava A, Conti L, Nelis S, Zhang C, Florance H, et al. Stability of small ubiquitin-like modifier (SUMO) proteases OVERLY TOLERANT TO SALT1 and -2 modulates salicylic acid signalling and SUMO1/2 conjugation in Arabidopsis thaliana. J Exp Bot. 2016;67:353–63.
  56.Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R. SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 2009;583:1261–6.PubMed CrossRef
  57.Pontes O, Vitins A, Ream TS, Hong E, Pikaard CS, Costa-Nunes P. Intersection of small RNA pathways in Arabidopsis thaliana sub-nuclear domains. PLoS One. 2013;8, e65652.PubMed PubMedCentral CrossRef
  58.Carr JP. Tobacco mosaic virus. In: Talbot NJ, editor. Annual plant reviews volume 11: plant-pathogen interactions. Oxford: Blackwell; 2004. p. 27–67.
  59.Zhou T, Murphy AM, Lewsey MG, Westwood JH, Zhang H, González I, et al. Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection. J Gen Virol. 2014;95:1408–13.PubMed PubMedCentral CrossRef
  60.Berry JO, Nikolau BJ, Carr JP, Klessig DF. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985;5:2238–46.PubMed PubMedCentral CrossRef
  61.Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time PCR data. Neurosci Lett. 2003;339:62–6.PubMed CrossRef
  62.Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(t)) method. Methods. 2001;25:402–8.PubMed CrossRef
  63.Westwood JH, Lewsey MG, Murphy AM, Tungadi T, Bates A, Gilligan CA, et al. Interference with jasmonic acid-regulated gene expression is a general property of viral suppressors of RNA silencing but only partly explains virus-induced changes in plant-aphid interactions. J Gen Virol. 2014;95:733–9.PubMed PubMedCentral CrossRef
  64.Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem. 1976;72:248–54.PubMed CrossRef
  65.Pfeiffer P, Laquel P, Hohn T. Cauliflower mosaic virus replication complexes: characterisation of the associated enzymes and of the polarity of the DNA synthesised in vitro. Plant Mol Biol. 1984;3:261–70.PubMed CrossRef
  66.Lei Z, Anand A, Mysore KS, Sumner LW. Electroelution of intact proteins from SDS-PAGE gels and their subsequent MALDI-TOF MS analysis. Methods Mol Biol. 2007;355:353–63.PubMed
  67.Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–5.PubMed CrossRef
  68.Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979;76:4350–4.PubMed PubMedCentral CrossRef
  69.Blom N, Gammeltoft S, Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol. 1999;294:1351–62.PubMed CrossRef
  70.Radivojac P, Vacic V, Haynes C, Cocklin RR, Mohan A, Heyen JW, et al. Identification, analysis, and prediction of protein ubiquitination sites. Proteins: Struct Funct Bioinf. 2010;78:365–80.CrossRef
  
• 作者单位：Wing-Sham Lee (1) (4)
  Shih-Feng Fu (1) (3)
  Zheng Li (1)
  Alex M. Murphy (1)
  Elizabeth A. Dobson (1)
  Laura Garland (1)
  Srinivasa Rao Chaluvadi (2)
  Mathew G. Lewsey (1) (5)
  Richard S. Nelson (2)
  John P. Carr (1)
  
  1. Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK
  4. Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
  3. Department of Biology, National Changhua University of Education, 1 Jin-De Road, Changhua City, 500, Taiwan
  2. Plant Biology Division, Samuel Roberts Noble Foundation, Inc, 2510 Sam Noble Parkway, Ardmore, OK, 73401, USA
  5. Centre for AgriBioscience, Department of Animal, Plant and Soil Science, School of Life Science, La Trobe University, Bundoora, Australia
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Host RNA-dependent RNA polymerases (RDRs) 1 and 6 contribute to antiviral RNA silencing in plants. RDR6 is constitutively expressed and was previously shown to limit invasion of Nicotiana benthamiana meristem tissue by potato virus X and thereby inhibit disease development. RDR1 is inducible by salicylic acid (SA) and several other phytohormones. But although it contributes to basal resistance to tobacco mosaic virus (TMV) it is dispensable for SA-induced resistance in inoculated leaves. The laboratory accession of N. benthamiana is a natural rdr1 mutant and highly susceptible to TMV. However, TMV-induced symptoms are ameliorated in transgenic plants expressing Medicago truncatula RDR1.