Can the inclusion of uniconazole improve the effectiveness of acibenzolar-S-methyl in managing bacterial speck (Pseudomonas syringae pv. tomato) and bacterial spot (Xanthomonas gardneri) in tomato?

  • Cheryl L. TruemanEmail author
  • Steven A. Loewen
  • Paul H. Goodwin


There are reports of acibenzolar-S-methyl (ASM) having host fitness costs and variable levels of control of bacterial speck (Pseudomonas syringae pv. tomato) and bacterial spot (Xanthomonas gardneri) in tomato (Solanum lycopersicum). The plant growth regulator uniconazole (UNI) is associated with alleviating abiotic stress symptoms, and was tested as an additive to ASM to see if it would reduce ASM-associated fitness costs and improve the consistency of disease control. Field applied ASM (fASM) plus greenhouse applied UNI (gUNI) was less consistent than fASM alone, as the combination reduced disease incidence in only two of three years versus fASM alone that reduced disease incidence in three of three years. However, fASM alone never increased total yield compared to the non-treated control, whereas fASM+gUNI increased it in one of three years, which was not associated with changes in disease intensity or relative chlorophyll levels. Greenhouse applied ASM (gASM) plus gUNI reduced disease incidence in one of three years, whereas gASM alone was never effective. This is the first report that gASM can result in long term disease control reducing disease severity up to 13 weeks post-application, indicating long-term effects of gASM are possible. The lack of improved consistency for disease control or improved yield with ASM combined with UNI compared to ASM alone indicates that other additives need to be tested. Also, further research is needed to discover why the ASM + UNI combination did provide improvements under certain field conditions.


Systemic acquired resistance Solanum lycopersicum 



This work was supported with funding from the Ontario Ministry of Agriculture, Food and Rural Affairs – University of Guelph Partnership Program (P. Goodwin), the Ontario Tomato Research Institute (C. Trueman), Syngenta Canada (C. Trueman), and Valent Canada (C. Trueman).

Compliance with ethical standards

Conflict of interest

C. Trueman has received research grants from Syngenta Canada and Valent Canada, and C. Trueman and S. Loewen have received research grants from the Ontario Tomato Research Institute.

Research involving human participants and/or animals

This research did not involve human participants and/or animals.

Supplementary material

10658_2019_1824_MOESM1_ESM.doc (151 kb)
ESM 1 (DOC 151 kb)


  1. Abbasi, P. A., Khabbaz, S. E., Weselowski, B., & Zhang, L. (2015). Occurrence of copper-resistant strains and a shift in Xanthomonas spp. causing tomato bacterial spot in Ontario. Canadian Journal of Microbiology, 61(10), 753–761. Scholar
  2. Abo-Elyousr, K. A. M., & El-Hendawy, H. H. (2008). Integration of Pseudomonas fluorescens and acibenzolar-S-methyl to control bacterial spot disease of tomato. Crop Protection, 27(7), 1118–1124. Scholar
  3. Achuo, E. A., Prinsen, E., & Höfte, M. (2006). Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathology, 55(2), 178–186. Scholar
  4. Alexander, S. A., & Waldenmaier, C. M. (2003). Evaluation of fungicides for control of bacterial spot in staked tomatoes, 2002. Fungicide and Nematicide Tests, 58, V056.Google Scholar
  5. Al-Rumaih, M. M., & Al-Rumaih, M. M. (2007). Physiological response of two species of Datura to uniconazole and salt stress. Journal of Food, Agriculture and Environment, 5(3–4), 450–453.Google Scholar
  6. Baysal, Ö., Soylu, E. M., & Soylu, S. (2003). Induction of defence-related enzymes and resistance by the plant activator acibenzolar-S-methyl in tomato seedlings against bacterial canker caused by Clavibacter michiganensis ssp. michiganensis. Plant Pathology, 52(6), 747–753. Scholar
  7. Bowman, D. T. (2001). Common use of the CV: A statistical aberration in crop performance trials. The Journal of Cotton Science, 5(2), 137–141.Google Scholar
  8. Bubici, G., Amenduni, M., Colella, C., D'Amico, M., & Cirulli, M. (2006). Efficacy of acibenzolar-S-methyl and two strobilurins, azoxystrobin and trifloxystrobin, for the control of corky root of tomato and verticillium wilt of eggplant. Crop Protection, 25(8), 814–820.CrossRefGoogle Scholar
  9. Cavalcanti, F. R., Resende, M. L. V., Lima, J. P. M. S., Silveira, J. A. G., & Oliveira, J. T. A. (2006). Activities of antioxidant enzymes and photosynthetic responses in tomato pre-treated by plant activators and inoculated by Xanthomonas vesicatoria. Physiological and Molecular Plant Pathology, 68(4–6), 198–208. Scholar
  10. Colebrook, E. H., Thomas, S. G., Phillips, A. L., & Hedden, P. (2014). The role of gibberellin signalling in plant responses to abiotic stress. The Journal of Experimental Biology, 217(1), 67–75. Scholar
  11. Cuppels, D. A., & Elmhirst, J. (1999). Disease development and changes in the natural Pseudomonas syringae pv. tomato populations on field tomato plants. Plant Disease, 83(8), 759–764. Scholar
  12. Damicone, J. P., & Trent, M. A. (2003). Evaluation of spray programs for control of bacterial spot and bacterial speck of fresh-market tomato, 2002. Fungicide and Nematicide Tests, 58, V018.Google Scholar
  13. Duan, L., Guan, C., Li, J., Eneji, A. E., Li, Z., & Zhai, Z. (2008). Compensative effects of chemical regulation with uniconazole on physiological damages caused by water deficiency during the grain filling stage of wheat. Journal of Agronomy and Crop Science, 194(1), 9–14. Scholar
  14. Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209. Scholar
  15. Gianquinto, G., Sambo, P., & Borsato, D. (2006). Determination of SPAD threshold values for the optimisation of nitrogen supply in processing tomato. Acta Horticulturae, (700), 159–166.Google Scholar
  16. Gong, P., Zhang, J., Li, H., Yang, C., Zhang, C., Zhang, X., Khurram, Z., Zhang, Y., Wang, T., Fei, Z., & Ye, Z. (2010). Transcriptional profiles of drought-responsive genes in modulating transcription signal transduction, and biochemical pathways in tomato. Journal of Experimental Botany, 61(13), 3563–3575. Scholar
  17. Goodwin, P. H., Trueman, C. L., Loewen, S. A., & Tazhoor, R. (2017). Variation in the response of tomato (Solanum lycopersicum) breeding lines to the effects of benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester (BTH) on systemic acquired resistance and seed germination. Journal of Phytopathology, 165(10), 670–680. Scholar
  18. Graves, A. S., & Alexander, S. A. (2002). Managing bacterial speck and spot of tomato with acibenzolar-s-methyl in Virginia. Plant Health Progress, 3, 11. Scholar
  19. Griffin, K., Gambley, C., Brown, P., & Li, Y. (2017). Copper-tolerance in Pseudomonas syringae pv. tomato and Xanthomonas spp. and the control of diseases associated with these pathogens in tomato and pepper. A systematic literature review. Crop Protection, 96, 144–150. Scholar
  20. 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(4–6), 192–200. Scholar
  21. 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(11), 1226–1232. Scholar
  22. Huang, D., Wu, W., Abrams, S. R., & Cutler, A. J. (2008). The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. Journal of Experimental Botany, 59(11), 2991–3007.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Huang, C.-H., Vallad, G. E., Zhang, S., Wen, A., Balogh, B., Figueiredo, J. F. L., et al. (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(2), 221–227. Scholar
  24. Jones, J. B. (1991a). Bacterial speck. In J. B. Jones, J. P. Jones, R. E. Stall, & T. A. Zitter (Eds.), Compendium of tomato diseases (Vol. first, pp. 26-27). St. Paul: APS Press.Google Scholar
  25. Jones, J. B. (1991b). Bacterial spot. In J. B. Jones, J. P. Jones, R. E. Stall, & T. A. Zitter (Eds.), Compendium of tomato diseases (Vol. first, pp. 27). St. Paul: APS Press.Google Scholar
  26. 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(6), 755–762. Scholar
  27. Koike, S. T., Gladders, P., & Paulus, A. O. (2007). Bacterial spot. In Vegetable diseases: a colour handbook (Vol. first, pp. 332-333). London: Manson Publishing.Google Scholar
  28. Kunz, W., Schurter, R., & Maetzke, T. (1997). The chemistry of benzothiadiazole plant activators. Pesticide Science, 50(4), 275–282.<275::AID-PS593>3.0.CO;2-7.CrossRefGoogle Scholar
  29. Lange, H. W., Borsick Herman, M. A., & Smart, C. D. (2007). Comparing efficacy of foliar and soil treatments for bacterial speck of tomato, 2006. Plant Disease Management Reports, 1, V009.Google Scholar
  30. Lanna-Filho, R., Souza, R. M., & Alves, E. (2017). Induced resistance in tomato plants promoted by two endophytic bacilli against bacterial speck. Tropical Plant Pathology, 42(2), 96–108. Scholar
  31. LeBoeuf, J., Cuppels, D., Dick, J., Pitblado, R., Loewen, S., & Celetti, M. (2009). Bacterial diseases of tomato: Bacterial spot, bacterial speck, bacterial canker. Accessed 23 Feb 2012.
  32. Lewis Ivey, M. L., Mera, J. R., & Miller, S. A. (2004). Evaluation of fungicides and bactericides for the control of foliar and fruit diseases of processing tomatoes, 2004. Fungicide and Nematicide Tests, 60, V110.Google Scholar
  33. Liu, M., Yu, H., Zhao, G., Huang, Q., Lu, Y., & Ouyang, B. (2017). Profiling of drought-responsive microRNA and mRNA in tomato using high-throughput sequencing. BMC Genomics, 18(1), 481–481. Scholar
  34. 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(5), 481–488.CrossRefPubMedGoogle Scholar
  35. Lund, R. E. (1975). Tables for an approximate test for outliers in linear models. Technometrics, 17, 473–476.CrossRefGoogle Scholar
  36. Mahesaniya, A. (2002). Paclobutrazol and acibenzolar-S-methyl induced tomato seedling growth response and resistance to bacterial speck (Pseudomonas syringae pv. tomato). M.Sc. Thesis, University of Guelph. Guelph; Dept. of Horticultural Science.Google Scholar
  37. Maymoune, A., Adeline, P., Marie, T., Sophie, G., Sophie, C., Catherine, L., Claire, N., & Sonia, H. (2015). Impact of abiotic stresses on the protection efficacy of defence elicitors and on metabolic regulation in tomato leaves infected by Botrytis cinerea. European Journal of Plant Pathology, 142(2), 223–237. Scholar
  38. Miller, S. A., & Mera, J. R. (2008). Evaluation of fungicide and bactericides for the control of foliar and fruit diseases of processing tomatoes, 2008. Plant Disease Management Reports, V008.
  39. Miller, S. A., Lewis Ivey, M. L., & Mera, J. (2002). Evaluation of fungicides and plant activators for the control of foliar and fruit disease of processing tomatoes, 2001. Fungicide and Nematicide Tests, 57, V116.Google Scholar
  40. Miller, S. A., Lewis Ivery, M. L., & Mera, J. R. (2005). Evaluation of fungicides and bactericides for the control of foliar and fruit diseases of processing tomatoes, 2015. Fungicide and Nematicide Tests, 61, V079. Scholar
  41. Monti, L. M. (1980). The breeding of tomatoes for peeling. Acta Horticulturae, (100), 341–353.Google Scholar
  42. Nir, I. D. O., Moshelion, M., & Weiss, D. (2014). The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant, Cell & Environment, 37(1), 113–123. Scholar
  43. 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(7), 736–740.CrossRefPubMedGoogle Scholar
  44. Pethybridge, S. J., & Nelson, S. C. (2015). Leaf doctor: A new portable application for quantifying plant disease severity. Plant Disease, 99(10), 1310–1316. Scholar
  45. Pieterse, C. M. J., Leon-Reyes, A., Van der Ent, S., & Van Wees, S. C. M. (2009). Networking by small-molecule hormones in plant immunity. Nature Chemical Biology, 5(5), 308–316. Scholar
  46. Pimentel-Gomes, F. (2009). Curso de estatística experimental (15th ed.). Piracicaba: Fundação de Estudos Agrários Luiz de Queiroz.Google Scholar
  47. Pontes, N. D. C., Nascimento, A. D. R., Golynski, A., Maffia, L. A., Rogério de Oliveira, J., & Quezado-Duval, A. M. (2016). Intervals and number of applications of acibenzolar-s-methyl for the control of bacterial spot on processing tomato. Plant Disease, 100(10), 2126–2133. Scholar
  48. Rademacher, W. (2000). Growth retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 501–531. Scholar
  49. Ritchie, D. F. (2000). Bacterial spot of pepper and tomato. The Plant Health Instructor.
  50. 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(12), 1519–1526.CrossRefGoogle Scholar
  51. Senaratna, T., Mackay, C. E., McKersie, B. D., & Fletcher, R. A. (1988). Uniconazole-induced chilling tolerance in tomato and its relationship to antioxidant content. Journal of Plant Physiology, 133(1), 56–61.CrossRefGoogle Scholar
  52. Spoel, S. H., & Dong, X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology, 12(2), 89–100. Scholar
  53. Srivastava, L. M. (2002). Plant growth and development: Hormones and environment. Amsterdam: Academic Press.Google Scholar
  54. Stutts, L., Wang, Y., & Stapleton, A. E. (2018). Plant growth regulators ameliorate or exacerbate abiotic, biotic and combined stress interaction effects on Zea mays kernel weight with inbred-specific patterns. Environmental and Experimental Botany, 147, 179–188. Scholar
  55. Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., & Mittler, R. (2014). Abiotic and biotic stress combinations. The New Phytologist, 203(1), 32–43. Scholar
  56. Syngenta (2012). Actigard 50WG. Accessed March 15 2013.
  57. Taylor, S. L., Payton, M. E., & Raun, W. R. (1999). Relationship between mean yield, coefficient of variation, mean square error, and plot size in wheat field experiments. Communications in Soil Science and Plant Analysis, 30(9), 1439–1447. Scholar
  58. Trueman, C. L. (2015). Copper alternatives for management of bacterial spot (Xanthomonas gardneri) and bacterial speck (Pseudomonas syringae pv. tomato) in processing tomatoes. Acta Horticulturae, 1069, 7.Google Scholar
  59. Valent (n.d.). SUMAGIC plant growth regulator. Accessed April 9 2019.
  60. Vallad, G. E., & Huang, C. H. (2011). Evaluation of copper and non-copper bactericides for the management of bacterial spot of tomato, spring 2011. Plant Disease Management Reports, 6, V034. Scholar
  61. van der Merwe, J. A., & Dubery, I. A. (2006). Benzothiadiazole inhibits mitochondrial NADH:Ubiquinone oxidoreductase in tobacco. Journal of Plant Physiology, 163, 877–882. Scholar
  62. Van Eerd, L. L., & Loewen, S. A. (2009) Prior winter wheat straw management influences processing tomato yield but not quality. In (823 ed., pp. 121–126): International Society for Horticultural Science (ISHS), Leuven.
  63. Villavicencio, L. E., Bethke, J. A., & Corkidi, L. (2015). Effect of uniconazole on the control of plant height and fruit yield of potted tomato, pepper, and eggplant. Horttech, 25(4), 522–527. Scholar
  64. Walters, D., & Heil, M. (2007). Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology, 71(1–3), 3–17. Scholar
  65. Wendehenne, D., Durner, J., Chen, Z. X., & Klessig, D. F. (1998). Benzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidase. Phytochemistry, 47(4), 651–657. Scholar
  66. Wilson, M., Campbell, H. L., Ji, P., Jones, J. B., & Cuppels, D. A. (2002). Biological control of bacterial speck of tomato under field conditions at several locations in North America. Phytopathology, 92(12), 1284–1292. Scholar
  67. Yunis, H., Bashan, Y., Okon, Y., & Henis, Y. (1980). Weather dependence, yield losses, and control of bacterial speck of tomato caused by Pseudomonas tomato. Plant Disease, 64, 937–939.CrossRefGoogle Scholar
  68. Zandstra, J., Dick, J., & Lang, J. (2006). Effect of plant growth regulators on tomato plug plant production, field establishment, maturity, yield & quality. Canadian Journal of Plant Science, 86(5), 1436–1436.Google Scholar
  69. Zhang, M., Duan, L., Tian, X., He, Z., Li, J., Wang, B., & Li, Z. (2007). Uniconazole-induced tolerance of soybean to water deficit stress in relation to changes in photosynthesis, hormones and antioxidant system. Journal of Plant Physiology, 164(6), 709–717. Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2019

Authors and Affiliations

  1. 1.Department of Plant Agriculture, Ridgetown CampusUniversity of GuelphRidgetownCanada
  2. 2.Ridgetown CampusUniversity of GuelphRidgetownCanada
  3. 3.School of Environmental SciencesUniversity of GuelphGuelphCanada

Personalised recommendations