Interactive effects of salicylic acid and jasmonic acid on secondary metabolite production in Echinacea purpurea

Abstract

Secondary metabolites are highly beneficial to human health and have commercial and industrial values. So, this research aimed to study the effects of exogenous salicylic acid (SA) and jasmonic acid (JA) on some secondary metabolites in purple coneflower. A field experiment as a randomized complete block design with three replications was conducted in Shahrood, Iran. Treatments were the factorial arrangement of 3 SA (0, 0.5, and 1 millimole) and 4 JA concentrations (0, 5, 20, and 50 micromole). The non-linear regression procedure was employed to quantify the relation of these materials with each other. The results indicated that the SA effect on all ten measured secondary metabolites changed with changing the JA levels as there was the interaction between these elicitors. On average, most (7 out of 11) of the combined SA_JA levels up-regulated the production of secondary metabolites as compared to the plants not sprayed with SA and JA. In terms of average response to elicitation with 11 combined SA_JA levels, they ranked from higher to lower as the guaiacol peroxidase, hydrogen proxide (H2O2), polyphenol oxidase, glutathione S-transferase, superoxide dismutase, NADPH oxidase, total phenolic content, phenylalanine ammonia-lyase, anthocyanin, and flavonoid. A few secondary metabolites appeared to have a biphasic relationship with each other. For instance, over lower and medium values of NADPH oxidase activity, anthocyanin content increased linearly with increasing NADPH oxidase activity; over higher values of NADPH oxidase activity, it showed a plateau state.

Keywords

• Antioxidants
• Bioactive compounds
• Purple coneflower
• Regulatory hormones

References

1. Acharya, B.R., & Assmann, S.M. (2009). Hormone interactions in stomatal function. Plant Molecular Biology, 69, 451–462. https://doi.org/10.1007/s11103-008-9427-0
2. Agati, G., Brunetti, C., Fini, A., Gori, A., Guidi, L., Landi, M., Sebastiani, F., & Tattini, M. (2020). Are flavonoids effective antioxidants in plants? Twenty years of our investigation. Antioxidants, 9, 1098. https://doi.org/10.3390/antiox9111098
3. Angelini, R., & Federico, R. (1989). Histochemical evidence of polyamine oxidation and generation of hydrogen peroxide in the cell wall. Journal of Plant Physiology, 135, 212–217. https://doi.org/10.1016/S0176-1617(89)80179-8
4. Bagal, U.R., Leebens-mack, J.H., Lorenz, W.W., & Dean, J.F.D. (2012). The phenylalanine ammonia lyase (PAL) gene family shows a gymnosperm-specific lineage. BMC Genomics, 13, 1471–2164. https://doi.org/10.1186/1471-2164-13-S3-S1
5. Bandurska, H., & Stroiński, A. (2005). The effect of salicylic acid on barley response to water deficit. Acta Physiol. Plant., 27, 379–386. https://doi.org/10.1007/s11738-005-0015-5
6. Beauchamp, C., & Fridovich, M. (1971). Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Analytical Biochemistry, 44, 276 287. https://doi.org/10.1016/0003-2697(71)90370-8
7. Bolwell, G.P., Bindschedler, L.V., Blee, K.A., Butt, V.S., Davies, D.R., Gardner, S.L., Gerrish, C., & Minibayeva, F. (2002). The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. Journal of Experimental Botany, 53, 1367–1376. https://doi.org/10.1093/jexbot/53.372.1367
8. Chance, B., & Maehly, A.C. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 11, 764–755. https://doi.org/10.1002/9780470110171.ch14

9. Chang, C., Yang, M., Wen, H., & Chern, J. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10, 178–182. https://doi.org/10.38212/2224-6614.2748
10. Dong, J., Wan, G., & Liang, Z. (2010). Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. Journal of Biotechnology, 148, 99 104. https://doi.org/10.1016/j.jbiotec.2010.05.009
11. Estévez, I.H., & Hernández, M.R. (2020). Plant glutathione S-transferases: an overview. Plant Gene, 23, 100233. https://doi.org/10.1016/j.plgene.2020.100233
12. Gholipoor, M., Emamgholizadeh, S., Hassanpour, H., Shahsavani, D., Shahoseini, H., Baghi, M., & Karimi, A. (2012). The optimization of root nutrient content for increased sugar beet productivity using an artificial neural network. International Journal of Plant Production, 6, 429–442. https://doi.org/10.22069/IJPP.2012.758
13. Gholipoor, M., Rohani, A., & Torani, S. (2013). Optimization of traits to increasing barley grain yield using an artificial neural network. International Journal of Plant Production, 7, 1–18. https://doi.org/10.22069/IJPP.2012.918
14. Gholipoor, M., & Nadali, F. (2019). Fruit yield prediction of pepper using artificial neural network. Scientia Horticulturae, 250, 249 253. https://doi.org/10.1016/j.scienta.2019.02.040
15. Gong, H., Jiao, Y., Hu, W., & Pua, E. (2005). Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Molecular Biology, 57, 53–66. https://doi.org/10.1007/s11103-004-4516-1
16. Gronwald, J.W., & Plaisance, K.L. (1998). Isolation and characterization of glutathione S-transferase isozymes from sorghum. Plant Physiology, 117, 877 892. https://doi.org/10.1104/pp.117.3.877
17. Ho, T.T., Murthy, H.N., & Park, S.Y. (2020). Methyl jasmonate induced oxidative stress and accumulation of secondary metabolites in plant cell and organ cultures. International Journal of Molecular Sciences, 21, 716. https://doi.org/10.3390/ijms21030716
18. Horváth, E., Csiszár, J., Gallé, Á., Poór, P., Szepesi, Á., & Tari, I. (2015). Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress. Journal of Plant Physiology, 183, 54 63. https://doi.org/10.1016/j.jplph.2015.05.010
19. Hu, X., Bidney, D.L., Yalpani, N., Duvick, J.P., Crasta, O., Folkerts, O., & Guihua, L. (2003). Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology, 133, 170 181. https://doi.org/10.1104/pp.103.024026
20. Kaiser, C., Geneve, R., & Ernst, M. (Eds.) (2015). Echinacea. Cooperative Extension Service, University of Kentucky, USA.
21. Kar, M., & Mishra, D. (1976). Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiology, 57, 315–319. https://doi.org/10.1104/pp.57.2.315
22. Karpets, Y.V., Kolupaev, Y.E., Lugovaya, A.A., & Oboznyi, A.I. (2014). Effect of jasmonic acid on the pro-/antioxidant system of wheat coleoptiles as related to hyperthermia tolerance. Russian Journal of Plant Physiology, 61, 339 346. https://doi.org/10.1134/S102144371402006X
23. Ketabchi, S., Majzoob, S., & Charegani, H.A. (2015). Effect of salicylic acid and methyl jasmonate on phenylalanine ammonia-lyase activity and total phenol in wheat infected by Pratylenchus thornei. Archives of Phytopathology and Plant Protection, 48, 10–17. https://doi.org/10.1080/03235408.2014.882104
24. Kolupaeva, Y.E., & Yastreb, T.O. (2021). Jasmonate signaling and plant adaptation to abiotic stressors (review). Applied Biochemistry and Microbiology, 57, 1 19. https://doi.org/10.1134/S0003683821010117
25. Kumari, G.J., Reddy, A.M., Naik, S.T., Kumar, S.G., Prasanthi, J., Sriranganayakulu, G., Reddy, P.C., & Sudhakar C. (2006). Jasmonic acid induced changes in protein pattern, antioxidative enzyme activities and peroxidase enzymes in peanut seedlings. Biologia Plantarum, 50, 219–226. https://doi.org/10.1007/s10535-006-0010-8
26. Manivannan, A., Soundararajan, P., Park, Y.G., & Jeong, B.R. (2016). Chemical elicitor-induced modulation of antioxidant metabolism and enhancement of secondary metabolite accumulation in cell suspension cultures of Scrophularia kakudensis Franch. International Journal of Molecular Sciences, 17, 399–412. https://doi.org/10.3390/ijms17030399
27. Mattioli, R., Francioso, A., Mosca, L., & Silva, P. (2020). Anthocyanins: a comprehensive review of their chemical properties and health effects on cardiovascular and neurodegenerative diseases. Molecules, 25, 3809. https://doi.org/10.3390/molecules25173809
28. Mendoza, D., Cuaspud, O., Ariasa, J.P., Ruiz, O., & Arias, M. (2018). Effect of salicylic acid and methyl jasmonate in the production of phenolic compounds in plant cell suspension cultures of Thevetia peruviana. Biotechnology Reports, 19, e00273. https://doi.org/10.1016/j.btre.2018.e00273
29. Mita, S., Murano, N., Akaike, M., & Nakamura, K. (1997). Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for beta-amylase and on the accumulation of anthocyanin that are inducible by sugars. Plant Journal, 11, 841–851. https://doi.org/10.1046/j.1365-313x.1997.11040841.x
30. Mohebby, M., Mortazavi, S.N., Kheiry, A., & Saba, J. (2021). Assessment of physiological and phytochemical traits of purple coneflower (Echinacea purpurea L. Moench) in response to salicylic acid and methyl jasmonate application. Medicinal Plant Research, 11, 1–13. https://doi.org/10.5376/mpr.2021.11.0001
31. Parsons, J.L., Cameron, S.I., Harris, C.S., & Smith, M.L. (2018). Echinacea biotechnology: advances, commercialization and future considerations. Pharmaceutical Biology, 56, 485–494. https://doi.org/10.1080/13880209.2018.1501583
32. Patel, T., Crouch, A., Dowless, K., & Freier, D. (2008). Acute effects of oral administration of a glycerol extract of Echinacea purpurea on peritoneal exudate cells in female swiss mice. Brain, Behavior and Immunology, 22, 39 49. https://doi.org/10.1016/j.bbi.2008.04.124
33. Rincón-Pérez, J., Rodríguez-Hernández, L., Ruíz-Valdiviezo, V.M., Abud-Archila, M., Luján-Hidalgo, M.C., Ruiz-Lau, N., González-Mendoza, D., & Gutiérrez-Miceli, F.A. (2016). Fatty acids profile, phenolic compounds and antioxidant capacity in elicited callus of Thevetia peruviana (Pers.) K. Schum. Journal of Oleo Science, 65, 311–318. https://doi.org/10.5650/jos.ess15254
34. Rouet, M., Mathieu, Y., Barbier-Brygoo, H., & Laurière, C. (2006). Characterization of active oxygen-producing proteins in response to hypo-osmolarity in tobacco and Arabidopsis cell suspensions: identification of a cell wall peroxidase. Journal of Experimental Botany, 57, 1323–1332. https://doi.org/10.1093/jxb/erj107
35. Sakamoto, M., & Suzuki, T. (2019). Methyl jasmonate and salinity increase anthocyanin accumulation in radish sprouts. Horticulturae, 5, 62 75. https://doi.org/10.3390/horticulturae5030062
36. Salehzadeh, H., Gholipoor, M., Abbasdokht, H., & Baradaran, M. (2016). Optimizing plant traits to increase yield quality and quantity in tobacco using artificial neural network. International Journal of Plant Production, 10, 97–108.
37. Schopfer, P., Heyno, E., Drepper, F., & Krieger-Liszkay, A. (2008). Naphthoquinone-dependent generation of superoxide radicals by quinone reductase isolated from the plasma membrane of soybean. Plant Physiology, 147, 864 878. https://doi.org/10.1104/pp.108.118745
38. Sharma, P., Jha, A.B., Dubey, R.S., & Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany, 2012, 217037. https://doi.org/10.1155/2012/217037
39. Singleton, V.L., & Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144–158.
40. Snell, F.D., & Snell, C.T. (1971). Colorometric Methods of Analysis. New York, Van Nostrand Reinhold.
41. Taranto, F., Pasqualone, A., Mangini, G., Tripodi, P., Miazzi, M.M., Pavan, S., & Montemurro, C. (2017). Polyphenol oxidases in crops: biochemical, physiological and genetic aspects. International Journal of Molecular Sciences, 18, 377 393. https://doi.org/10.3390/ijms18020377
42. Torun, H., Novák, O., Mikulík, J., Pěnčík, A., Strnad, M., & Ayaz, F.A. (2020). Timing-dependent effects of salicylic acid treatment on phytohormonal changes, ROS regulation, and antioxidant defense in salinized barley (Hordeum vulgare L.). Scientific Reports, 10, 13886. https://doi.org/10.1038/s41598-020-70807-3
43. Van-Gestelen, P., Asard, H., & Caubergs, R.J. (1997). Solubilization and separation of a plant plasma membrane NADPH-O2-synthase from other NAD(P)H oxidoreductases. Plant Physiology, 115, 543–550. https://doi.org/10.1104/pp.115.2.543
44. Wang, W., Wang, X., Huang, M., Cai, J., Zhou, Q., Dai, T., Cao, W., & Jiang, D. (2018). Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat. Frontiers in Plant Science, 9, 1137. https://doi.org/10.3389/fpls.2018.01137
45. Wang, J., Zheng, L., Wu, J., & Tan, R. (2006). Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide, 15, 351-358. https://doi.org/10.1016/j.niox.2006.04.261
46. Wasternack, C. (2014). Action of jasmonates in plant stress responses and development-Applied aspects. Biotechnology Advances, 32, 31 39. https://doi.org/10.1016/j.biotechadv.2013.09.009