Plant defense elicitor, 2, 4-dichloro-6-{(E)-[(3-methoxyphenyl) imino] methyl} phenol (DPMP) and its mode of action against fungal pathogen Alternaria solani in tomato (Solanum lycopersicum L.)

Abstract

Biotic stress factors are one of the major constraints plants face, and they significantly affect production and yield. There are multiple ways to cope with stress factors, including genetic enhancement. When they cannot provide sufficient protection, pesticides are commonly applied. Plant defense elicitors are a new approach for boosting plants' natural immune responses and tolerance levels. The newly identified promising plant defense elicitor; 2, 4-dichloro-6-{(E)-[(3-methoxyphenyl) imino] methyl} phenol (DPMP) was previously studied against the oomycete Hyaloperonospora arabidopsidis, the bacterial pathogens Pseudomonas syringae and Clavibacter michiganensis ssp michiganensis and found to induce disease resistance against these phytopathogens. However, it was not tested against fungal pathogens. Here for the first time, DPMP was evaluated against one of the most destructive fungal pathogens, Alternaria solani. Disease severity and plant development were evaluated. The results revealed that DPMP neither inhibited nor enhanced the disease severity of A. solani. Gene expression of several salicylic acid, jasmonic acid, and ethylene pathway-related genes (Pti4, TPK1b, Pto kinase, PRB1‐2, SABP2, and PR3) were also analyzed. According to the results, while DPMP induces PRB1-2, TPK1b, and Pto kinase gene expressions, the protection against A. solani does not occur via these genes. PR3 is one of the most important genes for defense responses against necrotrophic pathogens, and DPMP downregulated gene expression of PR3. These results demonstrated that DPMP mostly takes a role through the SA-related defense pathway and was effective against biotrophic and hemibiotrophic pathogens. However, it is not suitable for protection against the necrotrophic pathogen A. solani. Further research may pinpoint the activity of DPMP on the defense pathway and provide a better understanding of the mode of action for DPMP and other plant elicitors for specific plant protection solutions.

Keywords

• Fungal pathogen
• Plant activator,
• A. solani,
• Plant immunity

References

1. Adhikari, P., Oh, Y., & Panthee, D. (2017). Current Status of Early Blight Resistance in Tomato: An Update. Int. J. Mol. Sci., 18(10), 2019. doi:10.3390/ijms18102019
2. Ali, S., Ganai, B. A., Kamili, A. N., Bhat, A. A., Mir, Z. A., Bhat, J. A., . . . Grover, A. (2018). Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol. Res., 212-213, 29-37. doi:https://doi.org/10.1016/j.micres.2018.04.008
3. Anisimova, O. K., Shchennikova, A. V., Kochieva, E. Z., & Filyushin, M. A. (2021). Pathogenesis-Related Genes of PR1, PR2, PR4, and PR5 Families Are Involved in the Response to Fusarium Infection in Garlic (Allium sativum L.). Int. J. Mol. Sci., 22(13). doi:10.3390/ijms22136688
4. Bektas, Y. (2021). The synthetic elicitors 2,6-dichloro-isonicotinic acid (INA) and 2,4-dichloro-6-{(E)-[(3-methoxyphenyl)imino]methyl}phenol (DPMP) enhances tomato resistance against bacterial canker disease with different molecular mechanisms. Physiological and Molecular Plant Pathology, 116, 101740. doi:10.1016/j.pmpp.2021.101740
5. Bektas, Y., & Eulgem, T. (2015). Synthetic plant defense elicitors. Front. Plant. Sci, 5, 804. doi:10.3389/fpls.2014.00804
6. Bektas, Y., Rodriguez-Salus, M., Schroeder, M., Gomez, A., Kaloshian, I., & Eulgem, T. (2016). The Synthetic Elicitor DPMP (2,4-dichloro-6-{(E)-[(3-methoxyphenyl)imino]methyl}phenol) Triggers Strong Immunity in Arabidopsis thaliana and Tomato. Sci. Rep., 6, 29554. doi:10.1038/srep29554
7. Boyno, G., Demir, S., & Akköprü, A. (2020). Domateste Alternaria solani (Ell. & G. Martin) Sor.’ye Karşı Bazı Endofit Bakterilerin Etkisi. Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi, 6(3), 469-477. doi:10.24180/ijaws.770380
8. Brouwer, S. M., Odilbekov, F., Burra, D. D., Lenman, M., Hedley, P. E., Grenville-Briggs, L., . . . Andreasson, E. (2020). Intact salicylic acid signalling is required for potato defence against the necrotrophic fungus Alternaria solani. Plant. Mol. Biol., 104(1-2), 1-19. doi:10.1007/s11103-020-01019-6

9. Cohen, Y., Vaknin, M., & Mauch-Mani, B. (2016). BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica, 44(4), 513-538. doi:10.1007/s12600-016-0546-x
10. Edreva, A. (2005). Pathogenesis-related proteins: research progress in the last 15 years. Gen. Appl. Plant. Physiol., 31(1-2), 105-124.
11. Foolad, M. R., Merk, H. L., & Ashrafi, H. (2008). Genetics, Genomics and Breeding of Late Blight and Early Blight Resistance in Tomato. Crit Rev Plant Sci., 27(2), 75-107. doi:10.1080/07352680802147353
12. Foolad, M. R., & Panthee, D. R. (2012). Marker-Assisted Selection in Tomato Breeding. Critical Reviews in Plant Sciences, 31(2), 93-123. doi:10.1080/07352689.2011.616057
13. Gerage, J. M., Meira, A. P. G., & da Silva, M. V. (2017). Food and nutrition security: pesticide residues in food. Nutrire, 42(1). doi:10.1186/s41110-016-0028-4
14. Gianinazzi, S., & Kassanis, B. (1974). Virus resistance induced in plants by polyacrylic acid. J. Gen. Virol., 23, 1–9. doi:10.1099/0022-1317-23-1-1
15. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43, 205-227. doi:10.1146/annurev.phyto.43.040204.135923
16. Gu, Y.-Q., Wildermuth, M. C., Chakravarthy, S., Loh, Y.-T., Yang, C., He, X., . . . Martin, G. B. (2002). Tomato Transcription Factors Pti4, Pti5, and Pti6 Activate Defense Responses When Expressed in Arabidopsis. Plant Cell, 14(4), 817-831. doi:10.1105/tpc.000794
17. Gu, Y. Q., Yang, C., Thara, V. K., Zhou, J., & Martin, G. B. (2000). Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell, 12(5), 771-786. doi:10.1105/tpc.12.5.771
18. Jindo, K., Evenhuis, A., Kempenaar, C., Pombo Sudré, C., Zhan, X., Goitom Teklu, M., & Kessel, G. (2021). Review: Holistic pest management against early blight disease towards sustainable agriculture. Pest Manag. Sci., 77(9), 3871-3880. doi:10.1002/ps.6320
19. Khan, N., Mishra, A., & Nautiyal, C. S. (2012). Paenibacillus lentimorbus B-30488r controls early blight disease in tomato by inducing host resistance associated gene expression and inhibiting Alternaria solani. Biological Control, 62(2), 65-74. doi:10.1016/j.biocontrol.2012.03.010
20. Kishimoto, K., Matsui, K., Ozawa, R., & Takabayashi, J. (2006). Analysis of defensive responses activated by volatile allo-ocimene treatment in Arabidopsis thaliana. Phytochemistry, 67(14), 1520-1529. doi:10.1016/j.phytochem.2006.05.027
21. Lai, Z., & Mengiste, T. (2013). Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr Opin Plant Biol, 16(4), 505-512. doi:10.1016/j.pbi.2013.06.014
22. Langcake, P., & Wickins, S. G. A. (1975). Studies on the Mode of Action of the Dichlorocyclopropane Fungicides : Effects of 2,2-Dichloro- 3,3-dimethyl Cyclopropane Carboxylic Acid on the Growth of Piricularia oryzae Cav. J. Gen. Microbiol, 88, 295-306.
23. 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(4), 402-408. doi:10.1006/meth.2001.1262
24. Metraux, J. P., Ahlgoy, P., Staub, T., Speich, J., Steinemann, A., Ryals, J., & Ward, E. (1991). Induced Systemic Resistance in Cucumber in Response to 2,6-Dichloro-Isonicotinic Acid and Pathogens. In H. Hennecke & D. Verma (Eds.), Advances in Molecular Genetics of Plant-Microbe Interactions Vol. 1 (Vol. 10, pp. 432-439): Springer Netherlands.
25. Metraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., . . . Inverardi, B. (1990). Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science, 250(4983), 1004-1006. doi:10.1126/science.250.4983.1004
26. Nehela, Y., Taha, N. A., Elzaawely, A. A., Xuan, T. D., A. Amin, M., Ahmed, M. E., & El-Nagar, A. (2021). Benzoic Acid and Its Hydroxylated Derivatives Suppress Early Blight of Tomato (Alternaria solani) via the Induction of Salicylic Acid Biosynthesis and Enzymatic and Nonenzymatic Antioxidant Defense Machinery. J. Fungi, 7(8), 663. doi:10.3390/jof7080663
27. Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., & Hens, L. (2016). Chemical Pesticides and Human Health: The Urgent Need for a New Concept in Agriculture. Front Public Health, 4, 148. doi:10.3389/fpubh.2016.00148
28. Oh, C.-S., & Martin, G. B. (2011). Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci, 16(3), 132-140. doi:https://doi.org/10.1016/j.tplants.2010.11.001
29. Onaga, G., & Wydra, K. (2016). Advances in Plant Tolerance to Biotic Stresses. In: Abdurakhmonov, I. Y. , (Ed.). Plant Genomics. IntechOpen. https://doi.org/10.5772/60746InTech.
30. Pandey, K. K., Pandey, P. K., Kalloo, G., & Banerjee, M. K. (2003). Resistance to early blight of tomato with respect to various parameters of disease epidemics. J. Gen. Plant Pathol., 69(6), 364-371. doi:10.1007/s10327-003-0074-7
31. Pretty, J. (2008). Agricultural sustainability: concepts, principles and evidence. Philos Trans R Soc Lond B Biol Sci, 363(1491), 447-465. doi:10.1098/rstb.2007.2163
32. Rao, E. S., Munshi, A. D., Sinha, P., & Rajkumar. (2007). Genetics of rate limiting disease reaction to Alternaria solani in Tomato. Euphytica, 159(1-2), 123-134. doi:10.1007/s10681-007-9464-9
33. Rasool, M., Akhter, A., & Haider, M. S. (2021). Molecular and biochemical insight into biochar and Bacillus subtilis induced defense in tomatoes against Alternaria solani. Sci. Hortic., 285, 110203. doi:10.1016/j.scienta.2021.110203
34. Ray, S., Mondal, S., Chowdhury, S., & Kundu, S. (2015). Differential responses of resistant and susceptible tomato varieties to inoculation with Alternaria solani. Physiol. Mol. Plant Pathol., 90, 78-88. doi:10.1016/j.pmpp.2015.04.002
35. Serrano, M., Hubert, D. a., Dangl, J. L., Schulze-Lefert, P., & Kombrink, E. (2010). A chemical screen for suppressors of the avrRpm1-RPM1-dependent hypersensitive cell death response in Arabidopsis thaliana. Planta, 231(5), 1013-1023. doi:10.1007/s00425-010-1105-1
36. Singh, A. K., Rai, N., Singh, R. K., Saha, S., Rai, R. K., & Singh, R. P. (2017). Genetics of resistance to early blight disease in crosses of wild derivatives of tomato. Sci. Hortic., 219, 70-78. doi:10.1016/j.scienta.2017.01.052
37. Sinha, M., Singh, R. P., Kushwaha, G. S., Iqbal, N., Singh, A., Kaushik, S., . . . Singh, T. P. (2014). Current Overview of Allergens of Plant Pathogenesis Related Protein Families. Sci. World J, 2014, 543195. doi:10.1155/2014/543195
38. Skevas, T., Oude Lansink, A. G. J. M., & Stefanou, S. E. (2013). Designing the emerging EU pesticide policy: A literature review. NJAS-Wagen J Life Sc, 64-65, 95-103. doi:10.1016/j.njas.2012.09.001
39. Smith, J. E., Mengesha, B., Tang, H., Mengiste, T., & Bluhm, B. H. (2014). Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming. BMC Genomics, 15(1), 334. doi:10.1186/1471-2164-15-334
40. Spletzer, M. E., & Enyedi, A. J. (1999). Salicylic Acid Induces Resistance to Alternaria solani in Hydroponically Grown Tomato. Phytopathology®, 89(9), 722-727. doi:10.1094/phyto.1999.89.9.722
41. Tripathi, D., Jiang, Y. L., & Kumar, D. (2010). SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-S-methyl in plants. FEBS Lett, 584(15), 3458-3463. doi:10.1016/j.febslet.2010.06.046
42. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., . . . Ryals, J. (1992). Acquired resistance in Arabidopsis. Plant Cell, 4(6), 645-656. doi:10.1105/tpc.4.6.645
43. Vernooij, B., Friedrich, L., Goy, p. a., Staub, T., Kessmann, H., & Ryals, J. (1995). 2,6-dicholoroisonicotinic acid-induced resistance to pathogens without the accumulation of Saliciylic acid. MPMI, 8(2), 228-234.
44. Villaverde, J. J., Sevilla-Morán, B., Sandín-España, P., López-Goti, C., & Alonso-Prados, J. L. (2014). Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. 70(1), 2-5. doi:10.1002/ps.3663
45. Walters, D. R., Ratsep, J., & Havis, N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot, 64(5), 1263-1280. doi:10.1093/jxb/ert026
46. Wang, Y., Feng, G., Zhang, Z., Liu, Y., Ma, Y., Wang, Y., . . . Niu, X. (2021). Overexpression of Pti4, Pti5, and Pti6 in tomato promote plant defense and fruit ripening. Plant Science, 302, 110702. doi:10.1016/j.plantsci.2020.110702
47. Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., . . . Ryals, J. a. (1991). Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell, 3(10), 1085-1094. doi:10.1105/tpc.3.10.1085
48. Watanabe, T., Igarashi, H., Matsumoto, K., Seki, S., Mase, S., & Sekizawa, Y. (1977). The Characteristics of Probenazole (Oryzemate) for the Control of Rice Blast. J Pestic Sci, 2, 291-296.
49. Zhou, J., Jia, F., Shao, S., Zhang, H., Li, G., Xia, X., . . . Shi, K. (2015). Involvement of nitric oxide in the jasmonate-dependent basal defense against root-knot nematode in tomato plants. Front Plant Sci, 6. doi:10.3389/fpls.2015.00193