Abstract
Para-aminobenzoic (PABA) is reported to induce resistance against a range of plant pathogens in different crops in a salicylic acid-dependent manner. However, factors affecting its efficacy are not well understood. Foliar PABA applications on tomato seedlings reduced lesion incidence caused by Pseudomonas syringae pv. tomato (Pst) in a dose-dependent manner in distal leaves up to 18 mM under controlled environment conditions, but only three out of six commercial processing tomato cultivars tested showed a response to PABA. Leaves in direct contact with 9 and 18 mM PABA of both PABA-responsive and PABA-nonresponsive cultivars showed phytotoxicity. In a PABA-responsive cultivar, one, two and three PABA applications were equally effective at reducing lesion incidence in distal leaves, but the duration of control only persisted for approximately 7 days. Although PABA application reduced lesion incidence in distal leaves, the Pst population in leaves was unaffected. Lesions on PABA-treated plants were larger than nontreated plants, and thus the proportion of leaf surface area with lesions was unaffected by PABA treatment. In in vitro assays, 18 and 72 mM PABA produced zones of inhibition against Pst 15 and 50% larger than the ethanol control, demonstrating direct antimicrobial effects of PABA. PABA application did not affect symptom development in a mixed infection of Pst or Xanthomonas spp. in one field experiment with a PABA-responsive cultivar. Further research is needed to understand why PABA was unsuccessful in the field before it is to be used as a practical disease management tool for foliar bacterial diseases of tomato.
Similar content being viewed by others
References
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. https://doi.org/10.1139/cjm-2015-0228.
Ahn, I.-P., Kim, S., Lee, Y.-H., & Suh, S.-C. (2007). Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiology, 143(2), 838–848. https://doi.org/10.1104/pp.106.092627.
Basset, G. J. C., Ravanel, S., Quinlivan, E. P., White, R., Giovannoni, J. J., Rébeillé, F., Nichols, B. P., Shinozaki, K., Seki, M., Gregory III, J. F., & Hanson, A. D. (2004). Folate synthesis in plants: The last step of the p-aminobenzoate branch is catalyzed by a plastidial aminodeoxychorismate lyase. The Plant Journal, 40(4), 453–461. https://doi.org/10.1111/j.1365-313X.2004.02231.x.
Baysal, O., Gursoy, Y. Z., Ornek, H., Cetinel, B., & da Silva, J. A. T. (2007). Enhanced systemic resistance to bacterial speck disease caused by Pseudomonas syringae pv. tomato by DL-beta-aminobutyric acid under salt stress. Physiological Plant, 129(3), 493–506. https://doi.org/10.1111/j.1399-3054.2006.00818.x.
Bekusarova, S. A., Bome, N. A., Weisfeld, L. I., Tzomatova, F. T., & Luschenko, G. V. (2013). On the effects of PABA on germination. In G. E. Zaikov, A. N. Goloshchapov, & A. V. Lobanov (Eds.), Progress in organic and physical chemistry structurs and mechanisms (pp. 253–206). Apple Academic Press Inc..
Cagri, A., Ustunol, Z., & Ryser, E. T. (2001). Antimicrobial, mechanical, and moisture barrier properties of low pH whey protein-based edible films containing p-aminobenzoic or sorbic acids. Journal of Food Science, 66(6), 865–870. https://doi.org/10.1111/j.1365-2621.2001.tb15188.x.
Crisan, M. E., Bourosh, P., Maffei, M. E., Forni, A., Pieraccini, S., Sironi, M., & Chumakov, Y. M. (2014). Synthesis, crystal structure and biological activity of 2-hydroxyethylammonium salt of p-Aminobenzoic acid. PLoS One, 9(7), e101892. https://doi.org/10.1371/journal.pone.0101892.
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. https://doi.org/10.1094/PDIS.1999.83.8.759.
Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209. https://doi.org/10.1146/annurev.phyto.42.040803.140421.
Gimenez-Ibanez, S., & Solano, R. (2013). Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Frontiers in Plant Science, 4, 72. https://doi.org/10.3389/fpls.2013.00072.
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. https://doi.org/10.1111/jph.12606.
Goodwin, P. H., Trueman, C., Loewen, S. A., & Tazhoor, R. (2018). Variation in the responsiveness of induced resistance against Pseudomonas syringae pv. tomato by Solanum lycopersicum treated with Para-aminobenzoic acid. Physiological and Molecular Plant Pathology, 104, 31–39. https://doi.org/10.1016/j.pmpp.2018.08.007.
Gorelova, V., Ambach, L., Rébeillé, F., Stove, C., & Van Der Straeten, D. (2017). Folates in plants: Research advances and progress in crop biofortification. [review]. Frontiers in Chemistry, 5(21), https://doi.org/10.3389/fchem.2017.00021.
Heinzseed (2021) HeinzSeed international brochure. Heinzseed. Retrieved February 5, 2021, from https://d36rz30b5p7lsd.cloudfront.net/372/studio/assets/v1611911409263_1054604699/2021%20HeinzSeed%20International%20Brochure.pdf. Accessed 5 Feb 2021
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. https://doi.org/10.1016/j.pmpp.2008.02.002.
Hoang, L., Song, K., Rhee, I., Kim, J., & Lee, S. (2007). Mechanism by which Bacillus-derived 2-aminobenzoic acid inhibits the growth of Arabidopsis thaliana roots. J. Plant Biol., 50(4), 514–516. https://doi.org/10.1007/BF03030692.
Huang, T.-C., Chang, M.-C., & Alexander, M. (1981). Effect of Protozoa on bacterial degradation of an aromatic compound. Applied and Environmental Microbiology, 41(1), 229–232.
Huang, C. H., Vallad, G. E., Wen, A., Balogh, B., Figueiredo, J. F. L., Behlau, F., 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.
Ishikawa, R., Shirouzu, K., Nakashita, H., Teraoka, T., & Arie, T. (2007). Control efficacy of validamycin A against Fusarium wilt correlated with the severity of phytotoxic necrosis formed on tomato tissues. Journal of Pesticide Science, 32(2), 83–88. https://doi.org/10.1584/jpestics.G06-37.
Kelman, A., & Cook, R. J. (1977). Plant pathology in the People's Republic of China. Annual Review of Phytopathology, 15(1), 409–429. https://doi.org/10.1146/annurev.py.15.090177.002205.
Lund, R. E. (1975). Tables for an approximate test for outliers in linear models. Technometrics, 17, 473–476.
Melotto, M., Underwood, W., Koczan, J., Nomura, K., & He, S. Y. (2006). Plant stomata function in innate immunity against bacterial invasion. Cell, 126(5), 969–980. https://doi.org/10.1016/j.cell.2006.06.054.
Oliver, R., & Hewitt, H. G. (2014). Chapter 4: Fungicide discovery. In Fungicides in Crop Protection (2nd ed., Pp. 38–69). C.A.B. International.
Osborn, D. (2012). Chapter 5 pesticides in modern agriculture. In Environmental impacts of modern agriculture (pp. 111–128). The Royal Society of Chemistry.
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. https://doi.org/10.1038/nchembio.164.
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. https://doi.org/10.1094/PDIS-11-15-1286-RE.
Quinlivan, E. P., Roje, S., Basset, G., Shachar-Hill, Y., Gregory III, J. F., & Hanson, A. D. (2003). The folate precursor p-aminobenzoate is reversibly converted to its glucose ester in the plant cytosol. The Journal of Biological Chemistry, 278, 20731–20737. https://doi.org/10.1074/jbc.M302894200.
Richards, R. M. E., Xing, D. K. L., & King, T. P. (1995). Activity of p-aminobenzoic acid compared with other organic acids against selected bacteria. The Journal of Applied Bacteriology, 78(3), 209–215. https://doi.org/10.1111/j.1365-2672.1995.tb05018.x.
Rico, A., & Preston, G. M. (2008). Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Molecular Plant-Microbe Interactions, 21(2), 269–282. https://doi.org/10.1094/MPMI-21-2-0269.
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(3), 262–268. https://doi.org/10.1002/ps.285.
Song, G. C., Choi, H. K., & Ryu, C.-M. (2013). The folate precursor Para-aminobenzoic acid elicits induced resistance against cucumber mosaic virus and Xanthomonas axonopodis. Annals of Botany, 111(5), 925–934. https://doi.org/10.1093/aob/mct049.
Summermatter, K., Sticher, L., & Metraux, J.-P. (1995). Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae. Plant Physiology, 108, 1379–1385. https://doi.org/10.1104/pp.108.4.1379.
Ton, J., Pieterse, C. M. J., & Van Loon, L. C. (2006). The relationship between basal and induced resistance in Arabidopsis. In S. Tuzun & E. Bent (Eds.), Multigenic and Induced Systemic Resistance in Plants (Vol. first, pp. 197-224). Springer.
Trueman, C. L., Loewen, S. A., & Goodwin, P. H. (2019). 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? European Journal of Plant Pathology, 155(3), 927–942. https://doi.org/10.1007/s10658-019-01824-w.
Vallad, G. E., Cooperband, L., & Goodman, R. M. (2003). Plant foliar disease suppression mediated by composted forms of paper mill residuals exhibits molecular features of induced resistance. Physiological and Molecular Plant Pathology, 63(2), 65–77. https://doi.org/10.1016/j.pmpp.2003.10.003.
Van Loon, L. C. (1997). Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology, 103(9), 753–765. https://doi.org/10.1023/A:1008638109140.
Vos, I. A., Moritz, L., Pieterse, C. M. J., & Van Wees, S. C. M. (2015). Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Frontiers in Plant Science, 6(639). https://doi.org/10.3389/fpls.2015.00639.
Walters, D. R., & Fountaine, J. M. (2009). Practical application of induced resistance to plant diseases: An appraisal of effectiveness under field conditions. The Journal of Agricultural Science, 147, 523–535. https://doi.org/10.1017/S0021859609008806.
Walters, D. R., & Heil, M. (2007). Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology, 71, 3–17. https://doi.org/10.1016/j.pmpp.2007.09.008.
Yang, S. Y., Park, M. R., Kim, I. S., Kim, Y. C., Yang, J. W., & Ryu, C.-M. (2011). 2-aminobenzoic acid of Bacillus sp. BS107 as an ISR determinant against Pectobacterium carotovorum subsp. carotovotrum SCC1 in tobacco. European Journal of Plant Pathology, 129(3), 371–378. https://doi.org/10.1007/s10658-010-9687-9.
Zhou, L., Ji, Y., Zeng, C., Zhang, Y., Wang, Z., & Yang, X. (2013). Aquatic photodegradation of sunscreen agent p-aminobenzoic acid in the presence of dissolved organic matter. Water Research, 47(1), 153–162. https://doi.org/10.1016/j.watres.2012.09.045.
Funding
This work was supported with funding from the Ontario Ministry of Agriculture, Food and Rural Affairs – University of Guelph Partnership Program (P. Goodwin).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure of potential conflicts of interest
The authors declare that they have no conflict of interest.
Research involving Human Participants and/or Animals: This research did not involve human participants and/or animals.
Supplementary Information
ESM 1
(DOC 1299 kb)
Rights and permissions
About this article
Cite this article
Trueman, C.L., Goodwin, P.H. Effects of para-aminobenzoic acid on bacterial speck symptom development and Pseudomonas syringae pv. tomato populations in tomato leaves. Eur J Plant Pathol 160, 717–730 (2021). https://doi.org/10.1007/s10658-021-02280-1
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-021-02280-1