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The relationship between the plant-encoded RNA-dependent RNA polymerase 1 and alternative oxidase in tomato basal defense against Tobacco mosaic virus

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Abstract

Salicylic acid (SA) plays a critical role in plant defense against pathogen attack. The SA-induced viral defense in plants is distinct from the pathways mediating bacterial and fungal defense, which is pathogenesis-related protein-independent but involves an RNA-dependent RNA polymerase 1 (RDR1)-mediated RNA silencing mechanism and/or an alternative oxidase (AOX)-associated defense pathway. However, the relationship between these two viral defense-related pathways remains unclear. In this study, Tobacco mosaic virus (TMV) inoculation onto Solanum lycopersicum (tomato) leaves induced a rapid induction of the SlAOX1a transcript level as well as the total and CN-resistant respiration at 0.5 dpi, followed by an increase in SlRDR1 gene expression at 1 dpi in the upper uninoculated leaves. Silencing SlRDR1 using virus-induced gene silencing system significantly reduced SlRDR1 expression and tomato defense against TMV but had no evident effect on SlAOX1a transcription. Conversely, silencing SlAOX1a not only effectively reduced the AOX1a transcript level, but also blocked the TMV-induced SlRDR1 expression and decreased the basal defense against TMV. Furthermore, the application of an exogenous AOX activator on empty vector-silenced control plants greatly induced the accumulation of SlRDR1 and SlAOX1a transcript and reduced TMV viral RNA accumulation, but failed to have such effects on SlRDR1-silenced plants. Moreover, RDR1-overexpressed transgenic Nicotiana benthamiana plants enhanced defense against TMV than the empty vector-transformed plants, but these effects were not affected by the exogenous AOX activator or inhibitor. These results indicate that RDR1 is involved in the AOX-mediated defense pathway against TMV infection and plays a crucial role in enhancing RNA silencing to limit virus systemic spread.

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Abbreviations

AA:

Antimycin A

AOX:

Alternative oxidase

CN:

Cyanide

CP:

Coat protein

EV:

Empty vector

F v/F m :

Maximum quantum yield of photosystem II

H2O2 :

Hydrogen peroxide

KCN:

Potassium cyanide

miETC:

Mitochondrial electron transport chain

NO:

Nitric oxide

PR:

Pathogenesis-related protein

RDR1:

RNA-dependent RNA polymerase

ROS:

Reactive oxygen species

SA:

Salicylic acid

SHAM:

Salicylhydroxamic acid

TMV:

Tobacco mosaic virus

UQ:

Ubiquinone

VIGS:

Virus-induced gene silencing

Φ PSII :

Photochemical quantum yield at photosystem II

References

  • Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280

    Article  CAS  PubMed  Google Scholar 

  • Chivasa S, Carr JP (1998) Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell 10:1489–1498

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chivasa S, Murphy AM, Naylor M, Carr JP (1997) Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:547–557

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575

    Article  CAS  Google Scholar 

  • Ekengren SK, Liu YL, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36:905–917

    Article  CAS  PubMed  Google Scholar 

  • Fu LJ, Shi K, Gu M, Zhou YH, Dong DK, Liang WS, Song FM, Yu JQ (2010) Systemic induction and role of mitochondrial alternative oxidase and nitric oxide in a compatible tomato-Tobacco mosaic virus interaction. Mol Plant Microbe Interact 23:39–48

    Article  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relation ship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophysica Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gilliland A, Singh DP, Hayward JM, Moore CA, Murphy AM, York CJ, Slator J, Carr JP (2003) Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol 132:1518–1528

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hannon GJ (2002) RNA interference. Nature 418:244–251

    Article  CAS  PubMed  Google Scholar 

  • Hunter LJR, Westwood JH, Heath G, Macaulay K, Smith AG, MacFarlane SA, Palukaitis P, Carr JP (2013) Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS One 8:e66530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee WS, Fu SF, Verchot-Lubicz J, Carr JP (2011) Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biol 11:41

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lennon AM, Neuenschwander UH, Ribas-Carbo M, Giles L, Ryals JA, Siedow JN (1997) The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco. Plant Physiol 115:783–791

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liao YWK, Shi K, Fu LJ, Zhang S, Li X, Dong DK, Jiang YP, Zhou YH, Xia XJ, Liang WS, Yu JQ (2012) The reduction of reactive oxygen species formation by mitochondrial alternative respiration in tomato basal defense against TMV infection. Planta 235:225–238

    Article  CAS  PubMed  Google Scholar 

  • Liao YWK, Sun ZH, Zhou YH, Shi K, Li X, Zhang GQ, Xia XJ, Chen ZX, Yu JQ (2013) 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 8:e76090

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Millenaar FF, Gonzalez-Meler MA, Siedow JN, Wagner AM, Lambers H (2002) Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots. J Exp Bot 53:1081–1088

    Article  CAS  PubMed  Google Scholar 

  • Murphy AM, Chivasa S, Singh DP, Carr JP (1999) Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? Trends Plant Sci 4:155–160

    Article  PubMed  Google Scholar 

  • Nie WF, Wang MM, Xia XJ, Zhou YH, Shi K, Chen ZX, Yu JQ (2013) Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance. Plant Cell Environ 36:789–803

    Article  CAS  PubMed  Google Scholar 

  • Qu F (2010) Antiviral role of plant-encoded RNA-dependent RNA polymerases revisited with deep sequencing of small interfering RNAs of virus origin. Mol Plant Microbe Interact 23:1248–1252

    Article  CAS  PubMed  Google Scholar 

  • Rakhshandehroo F, Takeshita M, Squires J, Palukaitis P (2009) The influence of RNA-dependent RNA polymerase 1 on Potato virus Y infection and on other antiviral response genes. Mol Plant Microbe Interact 22:1312–1318

    Article  CAS  PubMed  Google Scholar 

  • Schiebel W, Pélissier T, Riedel L, Thalmeir S, Schiebel R, Kempe D, Lottspeich F, Sänger HL, Wassenegger M (1998) Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10:2087–2101

    PubMed Central  CAS  PubMed  Google Scholar 

  • Siddiqui SA, Sarmiento C, Truve E, Lehto H, Lehto K (2008) Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol Plant Microbe Interact 21:178–187

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wang X, Liu C, Zhang JD, Zhu CX, Gu XQ (2008) The NgAOX1a gene cloned from Nicotiana glutinosa is implicated in the response to abiotic and biotic stresses. Biosci Rep 28:259–266

    Article  PubMed  Google Scholar 

  • Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151

    Article  CAS  PubMed  Google Scholar 

  • Xie ZX, Fan BF, Chen CH, Chen ZX (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci USA 98:6516–6521

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang SJ, Carter SA, Cole AB, Cheng NH, Nelson RS (2004) A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc Natl Acad Sci USA 101:6297–6302

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JH, Seo HH, Han SJ, Yoon EK, Yang MS, Lee WS (2008) Phytohormone abscisic acid control RNA-dependent RNA polymerase 6 gene expression and post-transcriptional gene silencing in rice cells. Nucleic Acids Res 36:1220–1226

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu DQ, Fan BF, MacFarlane SA, Chen ZX (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant Microbe Interact 16:206–216

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Li YM, Li L, Yang JH, Zhang MF (2011) Ethylene is involved in leafy mustard systemic resistance to Turnip mosaic virus infection through the mitochondrial alternative oxidase pathway. Physiol Mol Plant Pathol 76:166–172

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31372108, 31071832), the National Key Technology R&D Program of China (2013AA102406), and the Fundamental Research Funds for the Central Universities of China.

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Correspondence to Kai Shi.

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Liao, YWK., Liu, YR., Liang, JY. et al. The relationship between the plant-encoded RNA-dependent RNA polymerase 1 and alternative oxidase in tomato basal defense against Tobacco mosaic virus . Planta 241, 641–650 (2015). https://doi.org/10.1007/s00425-014-2207-y

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  • DOI: https://doi.org/10.1007/s00425-014-2207-y

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