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Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker

Abstract

Soil application of the systemic insecticide imidacloprid (Admire®, Bayer Crop Science) produced season-long control of citrus canker caused by Xanthomonas citri sbsp. citri. Imidacloprid is a neo-nicotinoid that breaks down in planta into 6-chloronicotinic acid, a compound closely related to the systemic acquired resistance (SAR) inducer isonicotinic acid. Potted Swingle citrumelo seedlings (Citrus paradisi × Poncirus trifoliata) were treated with imidacloprid and the SAR inducers, isonicotinic acid, and acibenzolar-s-methyl as soil drenches or with acibenzolar-s-methyl as a foliar spray 1week prior to inoculation of immature leaves with X. citri sbsp. citri. Seedlings were re-inoculated four times over a 24-week period. SAR induction was confirmed by expression of the PR-2 gene (β-1,3 glucanase). Soil drenches of imidacloprid, isonicotinic acid, and acibenzolar-s-methyl induced a high and persistent up-regulation of PR-2 gene expression and reduced the number of canker lesions for up to 24 weeks compared to 4 weeks for foliar acibenzolar-s-methyl. Soil applied inducers of SAR reduced canker lesions up to 70% compared with the untreated inoculated plants. Lesions on leaves were small, necrotic, and flat compared to pustular lesions on inoculated untreated plants. Populations of X. citri sbsp. citri per leaf were reduced 1–3 log units in soil-treated plants compared to inoculated untreated plants.

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Abbreviations

ASM:

acibenzolar-s-methyl

Imid:

imidacloprid

INA:

isonicotinic acid

PR-2 :

pathogenicity-related protein 2

SAR:

systemic acquired resistance

SA:

salicylic acid

Xcc:

Xanthomonas citri sbsp. citri

References

  • Alva, A. K., Graham, J. H., & Anderson, C. A. (1995). Soil pH and copper effects on young ‘Hamlin’ orange trees. Soil Science Society of America Journal, 59, 481–487.

    CAS  Google Scholar 

  • Beckers, G. J., & Conrath, U. (2007). Priming for stress resistance: from the lab to the field. Current Opinion in Plant Biology, 10(4), 425–431.

    PubMed  Article  Google Scholar 

  • Bonasera, J. M., Kim, J. F., & Beer, S. V. (2006). PR genes of apple: identification and expression in response to elicitors and inoculation with Erwinia amylovora. BioMed Central Plant Biology, 6, 23.

    PubMed  Google Scholar 

  • Brisset, M. N., Cesbron, S., Thomson, S. V., & Paulin, J. P. (2000). Acibenzolar-S-methyl induces the accumulation of defence-related enzymes in apple and protects from fire blight. European Journal of Plant Pathology, 106(6), 529–536.

    Article  CAS  Google Scholar 

  • Cubero, J., & Graham, J. H. (2005). Quantitative real-time polymerase chain reaction for bacterial enumeration and allelic discrimination to differentiate Xanthomonas strains on citrus. Phytopathology, 95, 1333–1340.

    PubMed  Article  CAS  Google Scholar 

  • da Rocha, A. B., & Hammerschmidt, R. (2005). History and perspectives on the use of disease resistance inducers in horticultural crops. HortTechnology, 15(3), 518–529.

    Google Scholar 

  • Dekkers, M. G. H., Graham, J. H., Burns, J. K., Cubero, J., & Colburn, G. C. (2004). Evaluation of chemical inducers and PR protein reporters for induced systemic resistance to citrus bacterial diseases. Phytopathology, 94, S25.

    Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Gottwald, T. R., & Graham, J. H. (1992). A device for precise and nondisruptive stomatal inoculation of leaf tissue with bacterial pathogens. Phytopathology, 82, 930–935.

    Article  Google Scholar 

  • Gottwald, T. R., & Timmer, L. W. (1995). The efficacy of windbreaks in reducing the spread of citrus canker caused by Xanthamonas campestris pv. citri. Tropical Agriculture, 72, 194–201.

    Google Scholar 

  • Graham, J. H. (1998). Citrus Canker: control efforts in Brazil, prognosis for Florida. Citrus Industry, 79(8), 54–57.

    Google Scholar 

  • Graham, J. H., & Leite, R. P. (2004). Lack of control of citrus canker by induced systemic resistance compounds. Plant Disease, 88, 745–750.

    Article  CAS  Google Scholar 

  • Graham, J. H., & Leite, R. P., Jr. (2007). Soil applied neonicotinoids for control of bacterial diseases on young citrus trees. Proceedings of International Workshop on PR-Proteins and Induced Resistance Against Pathogens and Insects. Doorn, The Netherlands. p. 107.

  • Graham, J. H., Gottwald, T. R., Cubero, J., & Achor, D. S. (2004). Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Molecular Plant Pathology, 5(1), 1–15.

    Article  Google Scholar 

  • Graham, J. H., Gottwald, T. R., & Leite, R. P. (2006). Prospects for control of citrus canker with novel chemical compounds. Proceedings of Florida State Horticultural Society, 119, 82–88.

    Google Scholar 

  • Hammerschmidt, R., Métraux, J.-P., & van Loon, L. C. (2001). Inducing resistance: a summary of papers presented at the first international symposium on induced resistance to plant diseases, Corfu, May 2000. European Journal of Plant Pathology, 107, 1–6.

    Article  Google Scholar 

  • Kuhara, S. (1978). Present epidemic status and control of the citrus canker disease (Xanthomonas citri (Hasse) Dowson) in Japan. Review of Plant Protection Research, 11, 132–142.

    Google Scholar 

  • Leite, R. P., Jr. (1990). Cancro citrico - prevençao e controle no Parana. IAPAR, Londrina, PR, Brazil. Circular Number, 61.

  • Leite Jr., R. P., & Mohan, S. K. (1990). Integrated management of citrus bacterial canker disease caused by Xanthomonas campestris pv. citri in the State of Paraná, Brazil. Crop Protection, 9, 3–7.

    Article  Google Scholar 

  • Leite Jr., R. P., Mohan, S. K., Pereira, A. L. G., & Campaccci, C. A. (1987). Controle integrado de cancro cítrico - efeito da resistencia genética e da aplicaçao de bactericidas. Fitopatologia. Brásileira, 12, 257–263.

    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 

  • Maxson-Stein, K., He, S. Y., Hammerschmidt, R., & Jones, A. S. (2002). Effect of treating apple trees with Acibenzolar-S-Methyl on fire blight and expression of pathogenesis-related protein genes. Plant Disease, 86(7), 785–790.

    Article  CAS  Google Scholar 

  • McGuire, R. G. (1988). Evaluation of bactericidal chemicals for control of Xanthomonas campestris pv. vesicatoria that differ in sensitivity to copper. Plant Disease, 72, 1016–1020.

    Article  CAS  Google Scholar 

  • Muraro, R. P., Roka, F. M., & Spreen, T. H. (2002). Grower costs of having citrus canker in Florida with an overview of Argentina’s citrus canker control program. Department of Food and Resource Economics, University of Florida, IFAS, Gaineville. Staff Pap. SP02-3.

  • Rinaldi, D. A. M. F., & Leite Jr., R. P. (2000). Adaptation of Xanthomonas axonopodis pv. citri population to the presence of copper compounds in nature. Proceedings of the International Society of Citriculture, 2, 1064.

    Google Scholar 

  • Schubert, T. S., Rizvi, S. A., Sun, X., Gottwald, T. R., Graham, J. H., & Dixon, W. (2001). Meeting the challenge of eradicating citrus canker in Florida - again. Plant Disease, 85, 340–356.

    Article  Google Scholar 

  • Stall, R. E., Miller, J. W., Marcó, G. M., & Canteros de Echenique, B. I. (1980). Population dynamics of Xanthamonas citri causing cancrosis of citrus in Argentina. Proceedings of the Florida State Horticultural Society, 93, 10–14.

    Google Scholar 

  • Stall, R. E., Marcó, G. M., & Canteros de Echenique, B. I. (1982a). Importance of mesophyll in mature-leaf resistance to cancrosis of citrus. Phytopathology, 72, 1097–1100.

    Article  Google Scholar 

  • Stall, R. E., Miller, J. W., Marco, G. M., & Canteros de Echenique, B. I. (1982b). Timing of sprays to control cancrosis of grapefruit in Argentina. Proceedings of the International Society of Citriculture, 1, 414–417.

    Google Scholar 

  • Timmer, L. W. (1988). Evaluation of bactericides for control of citrus canker in Argentina. Proceedings of the Florida State Horticultural Society, 101, 6–9.

    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.

    PubMed  Article  Google Scholar 

  • Viloria, Z., Drouillard, D. L., Graham, J. H., & Grosser, J. W. (2004). Screening triploid hybrids of ‘Lakeland’ Limequat for resistance to citrus canker. Plant Disease, 88, 1056–1060.

    Article  Google Scholar 

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Acknowledgements

We thank to Alma Briseno, Maria Peacock and Diane Bright, (University of Florida, CREC) for their technical assistance, and Edwin Civerolo (USDA-ARS, Parlier, CA) and Zhonglin Mou (University of Florida, Gainesville) for suggestions in the revision of the manuscript.

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Correspondence to J. H. Graham.

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Francis, M.I., Redondo, A., Burns, J.K. et al. Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. Eur J Plant Pathol 124, 283–292 (2009). https://doi.org/10.1007/s10658-008-9415-x

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  • DOI: https://doi.org/10.1007/s10658-008-9415-x

Keywords

  • Gene expression
  • Pathogenicity-related proteins
  • Xanthomonas citri