Evaluation of acibenzolar-S-methyl-induced resistance against iris yellow spot tospovirus

Abstract

Acibenzolar-S-Methyl (ASM) is a functional analog of salicylic acid (SA) that activates local and systemic acquired resistance (SAR) responses in plants against a wide variety of pathogens. Iris yellow spot virus (IYSV) is an economically important tospovirus of onion that causes severe economic losses to both bulb and seed crops. IYSV resistant onion cultivars are not available to date and there are limited control options. To explore the possibility of utilizing SAR as a control option, we first used two different hosts of IYSV, Datura stramonium and Nicotiana benthamiana, to study the ability of ASM in triggering SAR against IYSV infection. Quantitative descriptors based on both symptom expression and relative levels of IYSV nucleoprotein and viral small RNA were developed and used to determine the SAR in ASM- and buffer-treated plants. A significant reduction in virus levels in ASM-treated plants was noticed by ELISA and PCR. The level of SAR response was also assessed by measuring the IYSV lesion size and number on the inoculated leaves of ASM-treated plants. ASM-treated plants showed reduced symptoms compared to buffer-treated plants. This study could be useful in potentially developing novel SAR-based options for virus management.

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References

  1. Anfoka, G. H. (2000). Benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester induces systemic resistance in tomato (Lycopersicon esculentum). Mill cv. Vollendung) to Cucumber mosaic virus. Crop Protection, 19(6), 401–405. doi:10.1016/S0261-2194(00)00031-4.

    CAS  Article  Google Scholar 

  2. Bag, S., & Pappu, H. R. (2009). Symptomatology of Iris yellow spot virus in selected indicator hosts. Plant Health Progress. doi:10.1094/PHP-2009-0824-01-BR.

    Google Scholar 

  3. Bag, S., Schwartz, H. F., Cramer, C. S., Havey, M. J., & Pappu, H. R. (2015). Iris yellow spot virus (Tospovirus: Bunyaviridae): from obscurity to research priority. Molecular Plant Pathology, 16, 224–37.

    CAS  PubMed  Article  Google Scholar 

  4. Benhamou, N., & Belanger, R. R. (1998). Induction of systemic resistance to Pythium damping-off in cucumber plants by benzothiadiazole: ultrastructure and cytochemistry of the host response. Plant Journal, 14(1), 13–21. doi:10.1046/j.1365-313X.1998.00088.x.

    CAS  PubMed  Article  Google Scholar 

  5. Boateng, C. O., & Schwartz, H. F. (2013). Temporal and localized distribution of iris yellow spot virus within tissues of infected onion plants. Southwestern Entomologist, 38(2), 183–200. doi:10.3958/059.038.0204.

    Article  Google Scholar 

  6. Campbell, H. L., & Wilson, M. (1999). Evaluation of actigard (CGA-245704) for the control of bacterial spot of peach. (Abstr.). Phytopathology, 89, S11.

    Article  Google Scholar 

  7. Chingandu, N. (2012). Investigating virus-host and virus-virus interactions using Iris yellow spot virus and Tomato spotted wilt virus (Tospovirus; Bunyaviridae) as model systems. Unpublished master’s thesis. Washington State University, Pullman, WA, USA.

  8. Chingandu, N., Druffel, K., Schroeder, K., Okubara, P., & Pappu, H. R. (2012). Quantitative molecular assays for investigating virus-host and virus-virus interactions using negative-stranded RNA viruses as a model system. Phytopathology, 102, S6–8.

    Google Scholar 

  9. Cole, D. L. (1999). The efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance, against bacterial and fungal diseases of tobacco. Crop Protection, 18(4), 267–273. doi:10.1016/S0261-2194(99)00026-5.

    CAS  Article  Google Scholar 

  10. Cortes, I., Livieratos, I. C., Derks, A., Peters, D., & Kormelink, R. (1998). Molecular and serological characterization of Iris yellow spot virus, a new and distinct tospovirus species. Phytopathology, 88(12), 1276–1282. doi:10.1094/phyto.1998.88.12.1276.

    CAS  PubMed  Article  Google Scholar 

  11. Cortes-Barco, A. M., Goodwin, P. H., & Hsiang, T. (2010). Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathology, 59(4), 643–653. doi:10.1111/j.1365-3059.2010.02283.x.

    CAS  Article  Google Scholar 

  12. Cramer, C., Singh, N., Kamal, N., & Pappu, H. R. (2014). Screening onion plant introduction accessions for tolerance to onion thrips and Iris yellow spot virus. HortScience, 49(10), 1253–1261.

    Google Scholar 

  13. Csinos, A. S., Pappu, H. R., McPherson, R. M., & Stephenson, M. G. (2001). Management of Tomato spotted wilt virus in flue-cured tobacco with acibenzolar-S-methyl and imidacloprid. Plant Disease, 85(3), 292–296. doi:10.1094/PDIS.2001.85.3.292.

    CAS  Article  Google Scholar 

  14. Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209. doi:10.1146/annurev.phyto.42.040803.140421.

    CAS  PubMed  Article  Google Scholar 

  15. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Rella, M. G., et al. (1996). A benzothiadiazole derivative induces systemic acquired resistance in tobacco. The Plant Journal, 10(1), 61–70. doi:10.1046/j.1365-313X.1996.10010061.x.

    CAS  Article  Google Scholar 

  16. Gent, D. H., Schwartz, H. F., & Khosla, R. (2004). Managing Iris yellow spot virus of onion with cultural practices, host genotype, and novel chemical treatments. (Abstr.). Phytopathology, 94, S34.

    Article  Google Scholar 

  17. Gent, D. H., du Toit, L. J., Fichtner, S. F., Mohan, S. K., Pappu, H. R., & Schwartz, H. F. (2006). Iris yellow spot virus: an emerging threat to onion bulb and seed production. Plant Disease, 90(12), 1468–1480. doi:10.1094/PD-90-1468.

    Article  Google Scholar 

  18. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., et al. (1996). Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. The Plant Cell Online, 8(4), 629–643. doi:10.1105/tpc.8.4.629.

    Article  Google Scholar 

  19. Hall, J. M., Mohan, K., Knott, E. A., & Moyer, J. W. (1993). Tospoviruses associated with scape blight of onion (Allium cepa) seed crops in Idaho. Plant Disease, 77, 952.

    Article  Google Scholar 

  20. Hammond-Kosack, K. E., & Jones, J. D. (1996). Resistance gene-dependent plant defense responses. Plant Cell, 8(10), 1773–1791.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  21. Hobbs, H. A., Black, L. L., Johnson, R. R., & Valverde, R. A. (1994). Difference in reactions among Tomato spotted wilt virus isolates to three resistant Capsicum chinense lines. Plant Disease, 78, 1220.

    Article  Google Scholar 

  22. Hoffmann, K., Qiu, W. P., & Moyer, J. W. (2001). Overcoming host- and pathogen-mediated resistance in tomato and tobacco maps to the M RNA of Tomato spotted wilt virus. Molecular Plant Microbe Interaction, 14(2), 242–249. doi:10.1094/mpmi.2001.14.2.242.

    CAS  Article  Google Scholar 

  23. Huang, Y. W., Hu, C. C., Liou, M. R., Chang, B. Y., Tsai, C. H., Meng, M., et al. (2012). Hsp90 interacts specifically with viral RNA and differentially regulates replication initiation of Bamboo mosaic virus and associated satellite RNA. PLoS Pathogens, 8(5), e1002726. doi:10.1371/journal.ppat.1002726.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. Ishii, H., Tomita, Y., Horio, T., Narusaka, Y., Nakazawa, Y., Nishimura, K., et al. (1999). Induced resistance of acibenzolar-S-methyl (CGA 245704) to cucumber and Japanese pear diseases. European Journal of Plant Pathology, 105(1), 77–85. doi:10.1023/A:1008637828624.

    CAS  Article  Google Scholar 

  25. Jensen, B. D., Olumide Latunde-Dada, A., Hudson, D., & Lucas, J. A. (1998). Protection of Brassica seedlings against downy mildew and damping-off by seed treatment with CGA 245704, an activator of systemic acquired resistance. Pesticide Science, 52(1), 63–69. doi:10.1002/(SICI)1096-9063(199801)52:1<63::AID-PS660>3.0.CO;2-2.

    CAS  Article  Google Scholar 

  26. Kritzman, A., Lampal, M., Raccah, B., & Gera, A. (2001). Distribution and transmission of Iris yellow spot virus. Plant Disease, 85, 838–842.

    Article  Google Scholar 

  27. Latham, L. J., & Jones, R. A. C. (1998). Selection of resistance breaking strains of Tomato spotted wilt tospovirus. Annals of Applied Biology, 133(3), 385–402. doi:10.1111/j.1744-7348.1998.tb05838.x.

    Article  Google Scholar 

  28. Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., et al. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant Journal, 10(1), 71–82.

    CAS  PubMed  Article  Google Scholar 

  29. Mandal, B., Mandal, S., Csinos, A. S., Martinez, N., Culbreath, A. K., & Pappu, H. R. (2008). Biological and molecular analyses of the acibenzolar-S-methyl-induced systemic acquired resistance in flue-cured tobacco against Tomato spotted wilt virus. Phytopathology, 98(2), 196–204. doi:10.1094/phyto-98-2-0196.

    CAS  PubMed  Article  Google Scholar 

  30. Momol, M. T., Olson, S. M., Funderburk, J. E., Stavisky, J., & Marois, J. J. (2004). Integrated Management of Tomato spotted Wilt on Field-Grown Tomatoes. Plant Disease, 88(8), 882–890. doi:10.1094/PDIS.2004.88.8.882.

    CAS  Article  Google Scholar 

  31. Morris, S. W., Vernooij, B., Titatarn, S., Starrett, M., Thomas, S., Wiltse, C. C., et al. (1998). Induced resistance responses in maize. Molecular Plant Microbe Interaction, 11(7), 643–658. doi:10.1094/mpmi.1998.11.7.643.

    CAS  Article  Google Scholar 

  32. Moury, B., Palloix, A., Gebre Selassie, K., & Marchoux, G. (1997). Hypersensitive resistance to Tomato spotted wilt virus in three Capsicum chinense accessions is controlled by a single gene and is overcome by virulent strains. Euphytica, 94(1), 45–52. doi:10.1023/A:1002997522379.

    Article  Google Scholar 

  33. Multani, P. S., Cramer, C. S., Steiner, R. L., & Creamer, R. (2009). Screening winter-sown onion entries for iris yellow spot virus tolerance. HortScience, 44(3), 627–632.

    Google Scholar 

  34. Novartis Crop Protection. (1999). Actigard, a new and novel plant health product for protection against diseases of agronomic, vegetable and tree crops. Novartis Crop Protection Technical Bulletin 4. Greensboro, NC.

  35. Pappu, H. R., Csinos, A. S., McPherson, R. M., Jones, D. C., & Stephenson, M. G. (2000). Effect of acibenzolar-S-methyl and imidacloprid on suppression of Tomato spotted wilt tospovirus in flue-cured tobacco. Crop Protection, 19(5), 349–354. doi:10.1016/S0261-2194 (00)00028-4.

    CAS  Article  Google Scholar 

  36. Pappu, H. R., du Toit, L. J., Schwartz, H. F., & Mohan, S. K. (2006). Sequence diversity of the nucleoprotein gene of Iris yellow spot virus (genus Tospovirus, family Bunyaviridae) isolates from the western region of the United States. Archive of Virology, 151(5), 1015–1023. doi:10.1007/s00705-005-0681-z.

    CAS  Article  Google Scholar 

  37. Pappu, H. R., Rosales, I. M., & Druffel, K. L. (2008). Serological and molecular assays for rapid and sensitive detection of iris yellow spot virus infection of bulb and seed onion crops. Plant Disease, 92(4), 588–594. doi:10.1094/PDIS-92-4-0588.

    CAS  Article  Google Scholar 

  38. Pappu, H. R., Jones, R. A., & Jain, R. K. (2009). Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Research, 141(2), 219–236. doi:10.1016/j.virusres.2009.01.009.

    CAS  PubMed  Article  Google Scholar 

  39. Ross, A. F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology, 14(3), 340–358. doi:10.1016/0042-6822(61)90319-1.

    CAS  PubMed  Article  Google Scholar 

  40. Ruess, W., Mueller, K., Kanuf-Beiter, G., Kunz, W., & Staub, T. (1996). Plant activator CGA 245704: An innovative approach for disease control in cereals and tobacco. Pages 53-60 in. Proc. Brighton Crop Prot. Conf. Pest Dis.

  41. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y., & Hunt, M. D. (1996). Systemic acquired resistance. The Plant Cell Online, 8(10), 1809–1819. doi:10.1105/tpc.8.10.1809.

    CAS  Article  Google Scholar 

  42. Sambrook, J., & Russell, D. W. (2001). In: molecular cloning: A laboratory manual (3rd ed.). Cold Spring Harbor: Cold Spring Harbor laboratory press.

    Google Scholar 

  43. Schwartz, H. F., Alston, D., Alwang, J., Bartolo, M., Blunt, T., et al. (2014). Onion ipmPIPE: a coordinated effort to improve the management of onion thrips and iris yellow spot virus for the U.S. Onion industry. Plant Health Progress. doi:10.1094/PHP-FE-14-0026.

    Google Scholar 

  44. Shock, C. C., Feibert, E., Jensen, L., Mohan, S. K., & Saunders, L. D. (2008). Onion variety response to iris yellow spot virus. HortTechnology, 18(3), 539–544.

    Google Scholar 

  45. Smith, T. N., Wylie, S. J., Coutts, B. A., & Jones, R. A. C. (2006). Localized distribution of iris yellow spot virus within leeks and its reliable large-scale detection. Plant Disease, 90(6), 729–733. doi:10.1094/PD-90-0729.

    Article  Google Scholar 

  46. Srinivasan, R., Sundaraj, S., Pappu, H. R., Diffie, S., Riley, D. G., & Gitaitis, R. D. (2012). Transmission of Iris yellow spot virus by Frankliniella fusca and Thrips tabaci (Thysanoptera: Thripidae). Journal of Economic Entomology, 105(1), 40–47.

    CAS  PubMed  Article  Google Scholar 

  47. Sticher, L., Mauch-Mani, B., & Metraux, J. P. (1997). Systemic acquired resistance. Annual Review of Phytopathology, 35, 235–270. doi:10.1146/annurev.phyto.35.1.235.

    CAS  PubMed  Article  Google Scholar 

  48. Tally, A., Oostendorp, M., Lawton, K., Staub, T., & Bassi, B. (1999). Commercial development of elicitors of induced resistance to pathogens. In A. A. Agrawal, S. Tuzun, & E. Bent (Eds.), Induced plant defenses against pathogens and herbivores: biochemistry, ecology, and agriculture (pp. 357–369). St. Paul: American Phytopathological Society (APS Press).

    Google Scholar 

  49. Tomlin, C. D. S. (2001). The pesticide manual (12th ed.). London: British Crop Protection Council.

    Google Scholar 

  50. Tripathi, D., Jiang, Y. L., & Kumar, D. (2010). SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-S-methyl in plants. FEBS Letters, 584(15), 3458–3463. doi:10.1016/j.febslet.2010.06.046.

    CAS  PubMed  Article  Google Scholar 

  51. Turina, M., Tavella, L., & Ciuffo, M. (2012). Chapter 12 - Tospoviruses in the Mediterranean Area. In Gad L, Hervé L, (Ed.), Advances in Virus Research. Academic Press, (84) 403-437.

  52. Vlot, A. C., Liu, P. P., Cameron, R. K., Park, S. W., Yang, Y., Kumar, D., et al. (2008). Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. The Plant Journal, 56(3), 445–456. doi:10.1111/j.1365-313X.2008.03618.x.

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

We thank Mrs. Nomatter Chingandu for her help with real-time PCR. Tripathi was supported by a research assistantship from the WSU Graduate Program in Molecular Plant Sciences. PPNS No. 0672, Department of Plant Pathology, College of Agricultural, Human and Natural Resource Sciences, Agricultural Research Center, Project # WNPO 0545, Washington State University, Pullman, WA 99164-6430, USA. This research was funded in part by the USDA-NIFA Specialty Crops Research Initiative SREP grant (2008-51180-04875).

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Tripathi, D., Pappu, H.R. Evaluation of acibenzolar-S-methyl-induced resistance against iris yellow spot tospovirus . Eur J Plant Pathol 142, 855–864 (2015). https://doi.org/10.1007/s10658-015-0657-0

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Keywords

  • Chemical inducers
  • Disease management
  • Disease resistance
  • Tospoviruses
  • Systemic acquired resistance