Skip to main content
SpringerLink
Log in

Soil applications of acibenzolar-S-methyl induce defense gene expression in tomato plants against bacterial spot

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Acibenzolar-S-methyl (ASM), a plant activator known to induce plant resistance, has been used as foliar sprays to manage several plant diseases including bacterial spot on tomato caused by four distinct Xanthomonas species. This study aimed to investigate the effects of soil application rates of ASM on bacterial spot of tomato and the expression levels of the two pathogenesis-related (PR) genes, PR1a and PR1b, in leaf tissues. Tomato seedlings were leaf-applied with ASM at 18.8 mg/l corresponding to the labeled rate, soil-applied with ASM at 0.84 and 10 mg/l, and sprayed with water served as an untreated control. The soil application of ASM at 10 mg/l consistently reduced the final disease severity and disease progress compared to the untreated control in four growth chamber experiments, whereas the soil application of ASM at 0.84 mg/l and foliar spray of ASM significantly reduced the final disease severity and area under disease progress curve (AUDPC) in three out of the four experiments. The expression levels of PR1a and PR1b in the leaf tissues were significantly induced by both soil and foliar applications of ASM. In addition, field trial results suggested that the soil applications of ASM at 10 mg/l markedly reduced disease progress compared to the control and copper standard. Although the control efficiency of soil applications of ASM depends on rates used, this study suggests that ASM can be used as soil applications to induce tomato resistance against bacterial spot.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barretti, P. B., Souza, R. M., Pozza, E. A., & Resende, M. L. V. (2010). Effect of application methods and dosages of acibenzolar-S-methyl on protection against bacterial wilt, pathogen populations, and growth of tomato plants. Tropical Plant Pathology, 35, 229–235.

    Google Scholar 

  • Block, A., Schmelz, E., O'Donnell, P. J., Jones, J. B., & Klee, H. J. (2005). Systemic acquired tolerance to virulent bacterial pathogens in tomato. Plant Physiology, 138, 1481–1490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209.

    Article  CAS  PubMed  Google Scholar 

  • Francis, M. I., Redondo, A., Burns, J. K., & Graham, J. H. (2009). Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. European Journal of Plant Pathology, 124, 283–292.

    Article  CAS  Google Scholar 

  • Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Rella, M. G., Meier, B., Dincher, S., Staub, T., Uknes, S., Metraux, J. P., Kessmann, H., & Ryals, J. (1996). A benzothiadiazole derivative induces systemic acquired resistance in tobacco. The Plant Jounal, 10, 61–70.

    Article  CAS  Google Scholar 

  • Graham, J. H., & Myers, M. E. (2011). Soil application of SAR inducers imidacloprid, thiamethoxam, and acibenzolar-S-methyl for citrus canker control in young grapefruit trees. Plant Disease, 95, 725–728.

    Article  CAS  Google Scholar 

  • Graham, J. H., & Myers, M. E. (2013). Integration of soil applied neonicotinoid insecticides and acibenzolar-S-methyl for systemic acquired resistance (SAR) control of citrus canker on young citrus trees. Crop Protection, 54, 239–243.

    Article  CAS  Google Scholar 

  • Herman, M. A. B., Restrepo, S., & Smart, C. D. (2007). Defense gene expression patterns of three SAR-induced tomato cultivars in the field. Physiological and Molecular Plant Pathology, 71, 192–200.

    Article  CAS  Google Scholar 

  • Herman, M. A. B., Davidson, J. K., & Smart, C. D. (2008). Induction of plant defense gene expression by plant activators and Pseudomonas syringae pv. tomato in greenhouse-grown tomatoes. Phytopathology, 98, 1226–1232.

    Article  CAS  PubMed  Google Scholar 

  • Hoagland, D. R., & Arnon, D. I. (1950) The water-culture method for growing plants without soil. Circular 347. University of California Agricultural Experiment Station, Berkley.

  • Horsfall, J. G. & Barratt, R. W. (1945) An improved grading system for measuring plant diseases. (Abstr.) Phytopathology, 35, 655.

  • Huang, C.-H., Vallad, G. E., Zhang, S., Wen, A., Balogh, B., Figueiredo, J. F. L., Behlau, F., Jones, J. B., Momol, M. T., & Olson, S. M. (2012). Effect of application frequency and reduced rates of acibenzolar-S-methyl on the field efficacy of induced resistance against bacterial spot on tomato. Plant Disease, 96, 221–227.

    Article  Google Scholar 

  • Johnson, K. B., & Temple, T. N. (2016). Comparison of methods of acibenzolar-S-methyl application for post-infection fire blight suppression in pear and apple. Plant Disease, 100, 1125–1131.

    Article  CAS  Google Scholar 

  • Johnson, K. B., & Temple, T. N. (2017). Induction of systemic acquired resistance aids restoration of tree health in field-grown pear and apple diseased with fire blight. Plant Disease, 101, 1263–1268.

    Article  Google Scholar 

  • Jones, J. B., Jones, J. P., Stall, J. P., & Zitter, T. A. (1991). Compendium of tomato diseases. St Paul: APS Press.

    Google Scholar 

  • Jones, J. B., Lacy, G. H., Bouzar, H., Stall, R. E., & Schaad, N. W. (2004). Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Systematic and Applied Microbiology, 27, 755–762.

    Article  CAS  PubMed  Google Scholar 

  • Jones, J. B., Momol, M. T., Obradovic, A., Balogh, B., & Olson, S. M. (2005). Bacterial spot management on tomatoes. Acta Horticulturae, 695, 119–124.

    Article  Google Scholar 

  • Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T., & Ryals, J. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. The Plant Journal, 10, 71–82.

    Article  CAS  PubMed  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Louws, F. J., Wilson, M., Campbell, H. L., Cuppels, D. A., Jones, J. B., Shoemaker, P. B., Sahin, F., & Miller, S. A. (2001). Field control of bacterial spot and bacterial speck of tomato using a plant activator. Plant Disease, 85, 481–488.

    Article  CAS  Google Scholar 

  • Marco, G. M., & Stall, R. E. (1983). Control of bacterial spot of pepper initiated by strains of Xanthomonas campestris pv. vesicatoria that differ in sensitivity to copper. Plant Disease, 67, 779–781.

    Article  CAS  Google Scholar 

  • Mascia, T., Santovito, E., Gallitelli, D., & Cillo, F. (2010). Evaluation of reference genes for quantitative reverse-transcription polymerase chain reaction normalization in infected tomato plants. Molecular Plant Pathology, 11, 805–816.

    Article  CAS  PubMed  Google Scholar 

  • Meller Harel, Y., Haile Mehari, Z., Rav-David, D., & Elad, Y. (2014). Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology, 104, 150–157.

    Article  Google Scholar 

  • Myresiotis, C. K., Vryzas, Z., & Papadopoulou-Mourkidou, E. (2014). Enhanced root uptake of acibenzolar-S-methyl (ASM) by tomato plants inoculated with selected Bacillus plant growth-promoting rhizobacteria (PGPR). Applied Soil Ecology, 77, 26–33.

    Article  Google Scholar 

  • Obradovic, A., Jones, J. B., Momol, M. T., Balogh, B., & Olson, S. M. (2004). Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Disease, 88, 736–740.

    Article  Google Scholar 

  • Obradovic, A., Jones, J. B., Momol, M. T., Olson, S. M., Jackson, L. E., Balogh, B., Guven, K., & Iriarte, F. B. (2005). Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Disease, 89, 712–716.

    Article  CAS  Google Scholar 

  • Olson, S. M., & Santos, B. S. (2010) Vegetable production handbook for Florida 2010–2011. Florida Cooperative Service, University of Florida.

  • Pernezny, K., Nagata, R., Havranek, N., & Sanchez, J. (2008). Comparison of two culture media for determination of the copper resistance of Xanthomonas strains and their usefulness for prediction of control with copper bactericides. Crop Protection, 27, 256–262.

    Article  CAS  Google Scholar 

  • Roberts, P. D., Momol, M. T., Ritchie, L., Olson, S. M., Jones, J. B., & Balogh, B. (2008). Evaluation of spray programs containing famoxadone plus cymoxanil, acibenzolar-S-methyl, and Bacillus subtilis compared to copper sprays for management of bacterial spot on tomato. Crop Protection, 27, 1519–1526.

    Article  CAS  Google Scholar 

  • Scarponi, L., Buonaurio, R., & Martinetti, L. (2001). Persistence and translocation of a benzothiadiazole derivative in tomato plants in relation to systemic acquired resistance against Pseudomonas syringae pv tomato. Pest Management Science, 57, 262–268.

    Article  CAS  PubMed  Google Scholar 

  • Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilizer on the expression of slow mildewing resistance in Knox wheat. Phytopathology, 67, 1051–1056.

    Article  CAS  Google Scholar 

  • Stall, R. E., Jones, J. B., & Minsavage, G. V. (2009). Durability of resistance in tomato and pepper to xanthomonads causing bacterial spot. Annual Review of Phytopathology, 47, 265–284.

    Article  CAS  PubMed  Google Scholar 

  • Takeshita, M., Okuda, M., Okuda, S., Hyodo, A., Hamano, K., Furuya, N., & Tsuchiya, K. (2013). Induction of antiviral responses by acibenzolar-S-methyl against cucurbit chlorotic yellows virus in melon. Phytopathology, 103, 960–965.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Tornero, P., Gadea, J., Conejero, V., & Vera, P. (1997). Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Molecular Plant-Microbe Interactions, 10, 624–634.

    Article  CAS  PubMed  Google Scholar 

  • van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology, 44, 135–162.

    Article  PubMed  Google Scholar 

  • Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3, research0034.1–0034.12.

  • Walters, D., Walsh, D., Newton, A., & Lyon, G. (2005). Induced resistance for plant disease control: Maximizing the efficacy of resistance elicitors. Phytopathology, 95, 1368–1373.

    Article  CAS  PubMed  Google Scholar 

  • Woodcock, J., Moazed, D., Cannon, M., Davies, J., & Noller, H. F. (1991). Interaction of antibiotics with A- and P-site-specific bases in 16S ribosomal RNA. The EMBO Journal, 10, 3099–3103.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, J. S., Reed, A., Chen, F., & Stewart, C. N. (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics, 7, 85.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported in part by a grant from the Ministry of Science and Technology, Taiwan, R.O.C. (MOST 104-2311-B-005-003-MY3) to C. -H. Huang. In addition, this study was partially funded through a USDA-AMS Specialty Crop Block Grant (grant number 018015) to the Florida Department of Agriculture and Consumer Services in partnership with the Florida Specialty Crop Foundation. We thank B. C. Hughes, C. M. Dyer, R. C. Willis, and H. M. Adkison for their technical assistance.

Author information

Authors and Affiliations

  1. Department of Soil and Environmental Sciences, National Chung Hsing University, 145 Xingda Rd., South Dist, Taichung City, 402, Taiwan

    Cheng-Hua Huang

  2. Gulf Coast Research and Education Center, University of Florida, IFAS, 14625 CR 672, Wimauma, FL, 33598, USA

    Gary E. Vallad

Authors
  1. Cheng-Hua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gary E. Vallad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gary E. Vallad.

Ethics declarations

Informed consent

All the authors carefully read and approved this version of the manuscript. Authors declare that this manuscript has not been published elsewhere, and that neither the data nor images have been manipulated. This article does not contain any research involving human participants and/or animals.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, CH., Vallad, G.E. Soil applications of acibenzolar-S-methyl induce defense gene expression in tomato plants against bacterial spot. Eur J Plant Pathol 150, 971–981 (2018). https://doi.org/10.1007/s10658-017-1336-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1336-0

Keywords

Search

Navigation