Abstract
Plant viruses cause many diseases that lead to significant economic losses. However, most of the approaches to control plant viruses, including transgenic processes or drugs are plant-species-limited or virus-species-limited, and not very effective. We introduce an application of jasmonic acid (JA) and salicylic acid (SA), a broad-spectrum, efficient and nontransgenic method, to improve plant resistance to RNA viruses. Applying 0.06 mM JA and then 0.1 mM SA 24 h later, enhanced resistance to Cucumber mosaic virus (CMV), Tobacco mosaic virus (TMV) and Turnip crinkle virus (TCV) in Arabidopsis, tobacco, tomato and hot pepper. The inhibition efficiency to virus replication usually achieved up to 80–90%. The putative molecular mechanism was investigated. Some possible factors affecting the synergism of JA and SA have been defined, including WRKY53, WRKY70, PDF1.2, MPK4, MPK2, MPK3, MPK5, MPK12, MPK14, MKK1, MKK2, and MKK6. All genes involving in the synergism of JA and SA were investigated. This approach is safe to human beings and environmentally friendly and shows potential as a strong tool for crop protection against plant viruses.
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Abbreviations
- JA:
-
Jasmonic acid
- SA:
-
Salicylic acid
- CMV:
-
Cucumber mosaic virus
- TMV:
-
Tobacco mosaic virus
- TCV:
-
Turnip crinkle virus
- TNV:
-
Tobacco necrosis virus
References
Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–971
Chan TY, Chan AY, Ho CS, Critchley JA (1995) The clinical value of screening for salicylates in acute poisoning. Vet Hum Toxicol 37:37–38
Clarke SM, Cristescu SM, Miersch O, Harren FJM, Wasternack C, Mur LAJ (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187
Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–1796
Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gutrella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250
Durrant WE, Dong XN (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng Y, Chen S, Li X, Yl Zhang (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6:34–44
He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell S, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115
Katz VA, Thulke OU, Conrath U (1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol 117:1333–1339
Kohlmeier JE, Woodland DL (2009) Immunity to respiratory viruses. Annu Rev Immunol 27:61–82
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331
Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar S (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567–577
Luo MH, Yuan S, Chen YE, Liu WJ, Du JB, Lei T, Wang MB, Lin HH (2009) Effects of salicylic acid on the photosystem II of barley seedlings under osmotic stress. Biol Plant 53:663–669
Manners JM, Penninckx IAMA, Vermaere K, Kazan K, Brown RL, Morgan A, Maclean DJ, Curtis MD, Cammue BPA, Broekaert WF (1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid. Plant Mol Biol 38:1071–1080
Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–830
Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513
Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262
Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116
Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis MAP Kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120
Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, MacKinlay J, Loake GJ, Mundy J, Morris PC (2008) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4 and MKS1. Plant Physiol 148:212–222
Rakwal R, Komatsu S (2001) Jasmonic acid-induced necrosis and drastic decreases in ribulose-1, 5-bisphosphate carboxylase/oxygenase in rice seedlings under light involves reactive oxygen species. J Plant Physiol 158:679–688
Shang J, Xi DH, Huang QR, Xu MY, Yuan S, Wang SD, Jia SD, Cao S, Zhou ZL, Lin HH (2009) Effect of two satellite RNAs on Nicotiana glutinosa infected with Cucumber mosaic virus (CMV). Physiol Mol Plant Pathol 74:184–190
Shang J, Xi DH, Yuan S, Xu F, Xu MY, Qi HL, Wang SD, Huang QR, Wen L, Lin HH (2010) Difference of physiological characters in dark green islands and yellow leaf tissue of CMV-infected Nicotiana tabacum leaves. Z Naturforsch 65c:73–78
Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D (2004) A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23:75–81
Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Pelt JAV, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van-Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770
Spoel SH, Mou Z, Tada Y, Spivey N, Genschik P, Dong XN (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–872
Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hasel S, Ikegamil M, Shah J (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45:803–809
Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl J, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152
Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104:1075–1080
Uquillas C, Letelier I, Blanco F, Jordana X, Holuigue L (2004) NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. Mol Plant Microbe Interact 17:34–42
Van Wees SC, de Swart EA, van Pelt JA, van Loon LC, Pieterse CM (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716
Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206
White NJ, Webster RG, Govorkova EA, Uyeki TM (2009) What is the optimal therapy for patients with H5N1 influenza? PLoS Med 6:e1000091
Yang YN, Qi M, Mei CS (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919
Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Z Naturforsch 63c:313–320
Acknowledgments
Arabidopsis thaliana seeds carrying NahG gene were gifts from Prof. Jia Li (University of Oklahoma, USA and Lanzhou University, China). Other Arabidopsis mutants were acquired from Arabidopsis Biological Resource Center (Ohio State University, Columbus, OH, USA). We thank Mr. Rupu Xiao (Certcana Systems Institute, Ontario, Canada) for the language edition. This work was supported by the National Key Basic Research ‘973’ Program of China (2009CB118500), National Nature Science Foundation of China (31070210, 30970214 and 30800071) and Sichuan Nature Science Foundation (2010JQ0080).
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Shang, J., Xi, DH., Xu, F. et al. A broad-spectrum, efficient and nontransgenic approach to control plant viruses by application of salicylic acid and jasmonic acid. Planta 233, 299–308 (2011). https://doi.org/10.1007/s00425-010-1308-5
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DOI: https://doi.org/10.1007/s00425-010-1308-5