Effectiveness of Hexanoic Acid for the Management of Bacterial Spot on Tomato Caused by Xanthomonas perforans
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals
2.2. Preparation of X. perforans Bacterial Suspension
2.3. In Vitro Assays
2.3.1. Determination of the MIC and MBC of Hexanoic Acid and Copper
2.3.2. Antibacterial Activity of Hexanoic Acid Against the Copper-Resistant Strain of X. perforans GEV 485
2.4. In Planta Assays
2.4.1. Effect of Hexanoic Acid on the Bacterial Spot of Tomato in the Greenhouse
2.4.2. Effect of Hexanoic Acid on the Development of Tomato Bacterial Spot and Yield in the Field
2.5. Statistical Analysis
3. Results
3.1. Determination of the MIC and MBC of Hexanoic Acid and Copper
3.2. Antibacterial Activity of Hexanoic Acid Against the Copper-Resistant Strain of X. perforans GEV 485
3.3. Effect of Hexanoic Acid on the Bacterial Spot of Tomato in the Greenhouse
3.4. Effect of Hexanoic Acid on the Development of Tomato Bacterial Spot and Yield in the Field
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- U.S. Department of Agriculture, National Agricultural Statistics Service. Vegetables 2023 Summary; 2024. Available online: https://usda.library.cornell.edu/concern/publications/02870v86p (accessed on 22 March 2025).
- Guan, Z.; Biswas, T.; Wu, F. The US Tomato Industry: An Overview of Production and Trade: FE1027. EDIS 2018, 2018. [Google Scholar] [CrossRef]
- Doidge, E.M. A Tomato Canker. Ann. Appl. Biol. 1921, 7, 407–430. [Google Scholar] [CrossRef]
- Strayer-Scherer, A.; Liao, Y.-Y.; Abrahamian, P.; Timilsina, S.; Paret, M.; Momol, T.; Jones, J.; Vallad, G.E. Integrated Management of Bacterial Spot on Tomato in Florida. In Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria; Springer: Berlin/Heidelberg, Germany, 2019; pp. 211–223. [Google Scholar] [CrossRef]
- Xanthomonas euvesicatoria pv. perforans (XANTPF) [World Distribution]. EPPO Global Database. Available online: https://gd.eppo.int/taxon/XANTPF/distribution (accessed on 22 March 2025).
- Osdaghi, E. Xanthomonas euvesicatoria pv. Perforans (Bacterial Spot of Tomato). CABI Compend. 2022. [Google Scholar] [CrossRef]
- Jones, J.B.; Lacy, G.H.; Bouzar, H.; Stall, R.E.; Schaad, N.W. Reclassification of the Xanthomonads Associated with Bacterial Spot Disease of Tomato and Pepper. Syst. Appl. Microbiol. 2004, 27, 755–762. [Google Scholar] [PubMed]
- Jibrin, M.O.; Timilsina, S.; Minsavage, G.V.; Vallad, G.E.; Roberts, P.D.; Goss, E.M.; Jones, J.B. Bacterial Spot of Tomato and Pepper in Africa: Diversity, Emergence of T5 Race, and Management. Front. Microbiol. 2022, 13, 835647. [Google Scholar] [CrossRef]
- Klein-Gordon, J.M.; Xing, Y.; Garrett, K.A.; Abrahamian, P.; Paret, M.L.; Minsavage, G.V.; Strayer-Scherer, A.L.; Fulton, J.C.; Timilsina, S.; Jones, J.B. Assessing Changes and Associations in the Xanthomonas perforans Population across Florida Commercial Tomato Fields via a Statewide Survey. Phytopathology 2021, 111, 1029–1041. [Google Scholar] [CrossRef]
- Potnis, N.; Timilsina, S.; Strayer, A.; Shantharaj, D.; Barak, J.D.; Paret, M.L.; Vallad, G.E.; Jones, J.B. Bacterial Spot of Tomato and Pepper: Diverse Xanthomonas Species with a Wide Variety of Virulence Factors Posing a Worldwide Challenge. Mol. Plant Pathol. 2015, 16, 907–920. [Google Scholar] [CrossRef]
- Liao, Y.Y.; Strayer-Scherer, A.L.; White, J.; Mukherjee, A.; de La Torre-Roche, R.; Ritchie, L.; Colee, J.; Vallad, G.E.; Freeman, J.H.; Jones, J.B.; et al. Nano-Magnesium Oxide: A Novel Bactericide against Copper-Tolerant Xanthomonas perforans Causing Tomato Bacterial Spot. Phytopathology 2019, 109, 52–62. [Google Scholar] [CrossRef]
- Ritchie, D.F.; Dittapongpitch, V. Copper- and Streptomycin-Resistant Strains and Host-Differentiated Races of Xanthomonas campestris pv. vesicatoria in North Carolina. Plant Dis. 1991, 75, 733–736. [Google Scholar] [CrossRef]
- Horvath, D.M.; Stall, R.E.; Jones, J.B.; Pauly, M.H.; Vallad, G.E.; Dahlbeck, D.; Staskawicz, B.J.; Scott, J.W. Transgenic Resistance Confers Effective Field-Level Control of Bacterial Spot Disease in Tomato. PLoS ONE 2012, 7, e42036. [Google Scholar] [CrossRef]
- Alva, A.K. Copper Contamination of Sandy Soils and Effects on Young Hamlin Orange Trees. Bull. Environ. Contam. Toxicol. 1993, 51, 857–864. [Google Scholar] [CrossRef] [PubMed]
- Zhu, B.; Alva, A.K. Trace Metal and Cation Transport in a Sandy Soil with Various Amendments. Soil Sci. Soc. Am. J. 1993, 57, 723–727. [Google Scholar] [CrossRef]
- Conover, R.A.; Gerhold, N.R. Mixtures of Copper and Maneb or Mancozeb for Control of Bacterial Spot of Tomato and Their Compatibility for Control of Fungal Diseases. Proc. Fla. State Hortic. Soc. 1981, 94, 154–156. [Google Scholar]
- Marco, G.M.; Stall, R.E. Control of Bacterial Spot of Pepper Initiated by Strains of Xanthomonas campestris pv. vesicatoria That Differ in Sensitivity to Copper. Plant Dis. 1983, 67, 779–781. [Google Scholar] [CrossRef]
- Worthington, R.J.; Rogers, S.A.; Huigens, R.W.; Melander, C.; Ritchie, D.F. Foliar-Applied Small Molecule That Suppresses Biofilm Formation and Enhances Control of Copper-Resistant Xanthomonas euvesicatoria on Pepper. Plant Dis. 2012, 96, 1638–1644. [Google Scholar] [CrossRef]
- Adhikari, P.; Adhikari, T.B.; Timilsina, S.; Meadows, I.; Jones, J.B.; Panthee, D.R.; Louws, F.J. Phenotypic and Genetic Diversity of Xanthomonas perforans Populations from Tomato in North Carolina. Phytopathology 2019, 109, 1533–1543. [Google Scholar] [CrossRef]
- Gullino, M.L.; Tinivella, F.; Garibaldi, A.; Kemmitt, G.M.; Bacci, L.; Sheppard, B. Mancozeb: Past, Present, and Future. Plant Dis. 2010, 94, 1076–1087. [Google Scholar] [CrossRef]
- Liu, Q.; Zhang, S.; Huang, Y.; Jones, J.B. Evaluation of a Small Molecule Compound 3-Indolylacetonitrile for Control of Bacterial Spot on Tomato. Crop Prot. 2019, 120, 7–12. [Google Scholar] [CrossRef]
- Qiao, K.; Liu, Q.; Xia, Y.; Zhang, S. Evaluation of a Small-Molecule Compound, N-Acetylcysteine, for the Management of Bacterial Spot of Tomato Caused by Copper-Resistant Xanthomonas perforans. Plant Dis. 2020, 105, 108–113. [Google Scholar] [CrossRef]
- Qiao, K.; Liu, Q.; Huang, Y.; Xia, Y.; Zhang, S. Management of Bacterial Spot of Tomato Caused by Copper-Resistant Xanthomonas perforans Using a Small Molecule Compound Carvacrol. Crop Prot. 2020, 132, 105114. [Google Scholar] [CrossRef]
- Pierre, K.; Liu, Q.; Jibrin, M.O.; Jones, J.B.; Zhang, S. Potential of Small Molecules Piperidine and Pyrrolidine Against Copper-Resistant Xanthomonas perforans, Causal Agent of Bacterial Spot of Tomato. Plant Dis. 2024. [Google Scholar] [CrossRef]
- Ward, G.E.; Carey, K.L.; Westwood, N.J. Using Small Molecules to Study Big Questions in Cellular Microbiology. Cell Microbiol. 2002, 4, 471–482. [Google Scholar] [CrossRef] [PubMed]
- Leyva, M.O.; Vicedo, B.; Finiti, I.; Flors, V.; Del Amo, G.; Real, M.D.; García-Agustín, P.; González-Bosch, C. Preventive and Post-Infection Control of Botrytis cinerea in Tomato Plants by Hexanoic Acid. Plant Pathol. 2008, 57, 1038–1046. [Google Scholar] [CrossRef]
- Vicedo, B.; Flors, V.; De La O Leyva, M.; Finiti, I.; Kravchuk, Z.; Real, M.D.; García-Agustín, P.; González-Bosch, C. Hexanoic Acid-Induced Resistance against Botrytis cinerea in Tomato Plants. Mol. Plant-Microbe Interact. 2009, 22, 1455–1465. [Google Scholar] [CrossRef]
- Llorens, E.; Scalschi, L.; Fernández-Crespo, E.; Lapeña, L.; García-Agustín, P. Hexanoic Acid Provides Long-Lasting Protection in ‘Fortune’ mandarin against Alternaria alternata. Physiol. Mol. Plant Pathol. 2015, 91, 38–45. [Google Scholar] [CrossRef]
- Llorens, E.; Camañes, G.; Lapeña, L.; García-Agustín, P. Priming by Hexanoic Acid Induces Activation of Mevalonic and Linolenic Pathways and Promotes the Emission of Plant Volatiles. Front. Plant Sci. 2016, 7, 495. [Google Scholar] [CrossRef]
- Kohler, A.; Schwindling, S.; Conrath, U. Benzothiadiazole-Induced Priming for Potentiated Responses to Pathogen Infection, Wounding, and Infiltration of Water into Leaves Requires the NPR1/NIM1 Gene in Arabidopsis. Plant Physiol. 2002, 128, 1046–1056. [Google Scholar] [CrossRef]
- Aranega-Bou, P.; de la O Leyva, M.; Finiti, I.; García-Agustín, P.; González-Bosch, C. Priming of Plant Resistance by Natural Compounds: Hexanoic Acid as a Model. Front. Plant Sci. 2014, 5, 488. [Google Scholar] [CrossRef]
- Finiti, I.; de la O Leyva, M.; Vicedo, B.; Gómez-Pastor, R.; López-Cruz, J.; García-Agustín, P.; Real, M.D.; González-Bosch, C. Hexanoic Acid Protects Tomato Plants Against Botrytis cinerea by Priming Defense Responses and Reducing Oxidative Stress. Mol. Plant Pathol. 2014, 15, 550–562. [Google Scholar] [CrossRef]
- Kravchuk, Z.; Vicedo, B.; Flors, V.; Camañes, G.; González-Bosch, C.; García-Agustín, P. Priming for JA-Dependent Defenses Using Hexanoic Acid Is an Effective Mechanism to Protect Arabidopsis against B. cinerea. J. Plant Physiol. 2011, 168, 359–366. [Google Scholar] [CrossRef]
- Llorens, E.; Vicedo, B.; López, M.M.; Lapeña, L.; Graham, J.H.; García-Agustín, P. Induced Resistance in Sweet Orange against Xanthomonas citri subsp. Citri by Hexanoic Acid. Crop Prot. 2015, 74, 77–84. [Google Scholar] [CrossRef]
- Horsfall, J.G.; Barratt, R.W. An Improved Grading System for Measuring Plant Diseases. Phytopathology 1945, 35, 655. [Google Scholar]
- Florida Automated Weather Network. Florida Automated Weather Network. University of Florida. Available online: https://fawn.ifas.ufl.edu/data/ (accessed on 22 March 2025).
- Zhang, S.; Fan, X.; Fu, Y.; Wang, Q.; McAvoy, E.; Seal, D.R. Field Evaluation of Tomato Cultivars for Tolerance to tomato chlorotic spot tospovirus. Plant Health Prog. 2019, 20, 77–82. [Google Scholar] [CrossRef]
- Agricultural Marketing Service. Tomato Grades and Standards. U.S. Department of Agriculture. Available online: https://www.ams.usda.gov/grades-standards/tomato-grades-and-standards (accessed on 22 March 2025).
- IBM Corp. IBM SPSS Statistics, Version 22; IBM Corp.: Armonk, NY, USA, 2013. [Google Scholar]
- SAS Institute Inc. SAS Software, Version 9.4; SAS Institute Inc.: Cary, NC, USA, 2013. [Google Scholar]
- Scalschi, L.; Vicedo, B.; Camañes, G.; Fernandez-Crespo, E.; Lapeña, L.; González-Bosch, C.; García-Agustín, P. Hexanoic Acid Is a Resistance Inducer That Protects Tomato Plants against Pseudomonas syringae by Priming the Jasmonic Acid and Salicylic Acid Pathways. Mol. Plant Pathol. 2013, 14, 342–355. [Google Scholar] [CrossRef]
- Behlau, F.; Canteros, B.I.; Minsavage, G.V.; Jones, J.B.; Graham, J.H. Molecular Characterization of Copper Resistance Genes from Xanthomonas citri subsp. Citri and Xanthomonas alfalfae subsp. Citrumelonis. Appl. Environ. Microbiol. 2011, 77, 4089–4096. [Google Scholar] [CrossRef]
- Mir, A.R.; Pichtel, J.; Hayat, S. Copper: Uptake, Toxicity, and Tolerance in Plants and Management of Cu-Contaminated Soil. Biometals 2021, 34, 737–759. [Google Scholar] [CrossRef]
- Neaman, A.; Schoffer, J.T.; Navarro-Villarroel, C.; Pelosi, C.; Peñaloza, P.; Dovletyarova, E.A.; Schneider, J. Copper Contamination in Agricultural Soils: A Review of the Effects of Climate, Soil Properties, and Prolonged Copper Pesticide Application in Vineyards and Orchards. Plant Soil Environ. 2024, 70, 407–417. [Google Scholar] [CrossRef]
- Hoang, T.C.; Rogevich, E.C.; Rand, G.M.; Gardinali, P.R.; Frakes, R.A.; Bargar, T.A. Copper Desorption in Flooded Agricultural Soils and Toxicity to the Florida Apple Snail (Pomacea paludosa): Implications in Everglades Restoration. Environ. Pollut. 2008, 154, 338–347. [Google Scholar] [CrossRef]
- Sigma-Aldrich. Hexanoic Acid, 98%; Product No. 153745. Sigma-Aldrich. Available online: https://www.sigmaaldrich.com/US/en/sds/aldrich/153745 (accessed on 22 March 2025).
- Enrique, R.; Siciliano, F.; Favaro, M.A.; Gerhardt, N.; Roeschlin, R.; Rigano, L.; Sendin, L.; Castagnaro, A.; Vojnov, A.; Maran, M.R. Novel Demonstration of RNAi in Citrus Reveals Importance of Citrus Callose Synthase in Defence Against Xanthomonas citri subsp. Citri. Plant Biotechnol. J. 2011, 9, 394–407. [Google Scholar] [CrossRef]
- Chen, K.; Li, G.-J.; Bressan, R.A.; Song, C.-P.; Zhu, J.-K.; Zhao, Y. Abscisic Acid Dynamics, Signaling, and Functions in Plants. J. Integr. Plant Biol. 2020, 62, 25–54. [Google Scholar] [CrossRef]
- Lamichhane, J.R.; Osdaghi, E.; Behlau, F.; Köhl, J.; Jones, J.B.; Aubertot, J.N. Thirteen Decades of Antimicrobial Copper Compounds Applied in Agriculture: A Review. Agron. Sustain. Dev. 2018, 38, 28. [Google Scholar] [CrossRef]
- Jibrin, M.O.; Liu, Q.; Jones, J.B.; Zhang, S. Surfactants in Plant Disease Management: A Brief Review and Case Studies. Plant Pathol. 2021, 70, 495–510. [Google Scholar] [CrossRef]
- Dawen, D.E.; Amienyo, C.A.; Okechalu, B.O.; Dapiya, H.; Kutshik, R.J. In Vitro and In Vivo Efficacy of Plant Extracts in the Control of Late Blight Disease of Potato Caused by Phytophthora infestans Mont. De Bary in Nigeria. Int. J. Plant Pathol. Microbiol. 2023, 3, 13–19. Available online: https://www.plantpathologyjournal.com/article/49/3-2-4-307.pdf (accessed on 22 March 2025).
- Talabac, M.; Ristvey, A.; Vollmer, K. Phytotoxicity and Chemical Damage to Garden Plants. Univ. Md. Ext. 2024. Available online: https://extension.umd.edu/resource/phytotoxicity-chemical-damage-garden-plants (accessed on 22 March 2025).
Hexanoic Acid and Copper Concentrations (mg/L) a | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Treatment | 16 | 32 | 64 | 128 | 256 | 512 | 1024 | 2048 | 4096 | 8192 |
Hexanoic Acid (HA) | + | + | + | + | + | MIC | MBC | - | - | - |
Copper (CuSO4) | + | + | + | + | + | + | MIC | MBC | - | - |
Trial 1 a | Trial 2 a | |||||
---|---|---|---|---|---|---|
Treatment | DS b (%) | AUDPC c | Yield d (kg/plant) | DS b (%) | AUDPC c | Yield d (kg/plant) |
Untreated control | 19.0 a | 212.6 a | 6.93 b | 49.4 a | 560.3 a | 2.85 a |
Hexanoic acid 0.5 g/L | 13.1 b | 122.0 b | 7.07 b | 44.2 b | 441.0 b | 2.72 a |
ManKocide 2.1 g/L | 10.8 c | 95.9 c | 8.83 a | 41.3 b | 390.1 c | 2.76 a |
LSD0.05 | 1.91 | 26.4 | 1.34 | 5.0 | 48.7 | 0.54 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pierre, K.; Thapa, N.; Liu, Q.; Jibrin, M.O.; Jones, J.B.; Zhang, S. Effectiveness of Hexanoic Acid for the Management of Bacterial Spot on Tomato Caused by Xanthomonas perforans. Agriculture 2025, 15, 695. https://doi.org/10.3390/agriculture15070695
Pierre K, Thapa N, Liu Q, Jibrin MO, Jones JB, Zhang S. Effectiveness of Hexanoic Acid for the Management of Bacterial Spot on Tomato Caused by Xanthomonas perforans. Agriculture. 2025; 15(7):695. https://doi.org/10.3390/agriculture15070695
Chicago/Turabian StylePierre, Ketsira, Naweena Thapa, Qingchun Liu, Mustafa Ojonuba Jibrin, Jeffrey B. Jones, and Shouan Zhang. 2025. "Effectiveness of Hexanoic Acid for the Management of Bacterial Spot on Tomato Caused by Xanthomonas perforans" Agriculture 15, no. 7: 695. https://doi.org/10.3390/agriculture15070695
APA StylePierre, K., Thapa, N., Liu, Q., Jibrin, M. O., Jones, J. B., & Zhang, S. (2025). Effectiveness of Hexanoic Acid for the Management of Bacterial Spot on Tomato Caused by Xanthomonas perforans. Agriculture, 15(7), 695. https://doi.org/10.3390/agriculture15070695