Influence of methyl jasmonate on expression patterns of polyketide synthase genes in Hypericum perforatum L.

Document Type : Original Article

Authors

1 Associate Professor, Department of Plant Production and Genetics, Faculty of Agriculture, University of Kurdistan, Sanandaj, Iran

2 MSc. graduate, Department of Plant Production and Genetics, Faculty of Agriculture, University of Kurdistan, Sanandaj, Iran

10.22034/plant.2024.141075.1091

Abstract

St. John's wort (Hypericum perforatum L.) is a medicinal plant that is well known for its anti-depressant properties. Hypericin and hyperforin are the two active compounds that have the greatest medicinal value. Considering the importance of these compounds, it is necessary to have solutions to increase their production through biotechnology. Therefore, as preliminary study the expression of two key polyketide synthase genes including HpPKS2 and HpPKS1 in hypericin biosynthetic pathway was studied. Methyl jasmonate was used as elicitor to stimulate gene expression in concentrations of 0, 10 and 100 micromolar before flowering stage. Leaves and stems samples were then collected at 0, 12, 24 and 48 hours after MeJA treatment. The expression level of genes was examined by semi-quantitative RT-PCR method. The results showed that the expression level of both HpPKS2 and HpPKS1 genes were increased in leaf and stem tissues due to the application of MeJA, and at the concentrations of 10 and especially 100 µm, there was a significant difference with the control (0 concentration). Moreover, the expression level of both genes showed a rising trend in the time series of 0, 12, 24 and 48 hours after spraying MeJA in both tissues, and generally the greatest increase in expression was observed at 48 hours. The results of this study showed that both polyketide synthase genes are induced under the influence of methyl jasmonate and lead to their higher expression.

Keywords


Barnes, J., Anderson, L. A., & Phillipson, J. D. (2001). St John’s wort (Hypericum perforatum L.): a review of its chemistry, pharmacology and clinical properties. Journal of Pharmacy and Pharmacology, 53, 583–600. doi: 10.1211/0022357011775910.
Bhaskar, R., Xavier, L.S.E., & Udayakumaran, G. (2022). Biotic elicitors: a boon for the in-vitro production of plant secondary metabolites. Plant Cell Tissue and Organ Culture, 149, 7–24. https://doi.org/10.1007/s11240-021-02131-1.
Bais, H.P., Walker, T.S., Stermitz, F.R., Hufbauer, R.A., & Vivanco, J.M. 2002b. Enantiomeric-dependent phytotoxic and antimicrobial activity of (±)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiology, 128, 1173-1179.
Baenas, N.; Garcia-Viguera, C.; Moreno, & Elicitation, D.A. (2014). A tool for enriching the bioactive composition of foods. Molecules, 2014, 19, 13541–13563.
Bunjan, W., Sujipuli, K., & Prasarnpun, S. (2018) Effect of methyl jasmonate elicitation on biomass, gene expression and saponin accumulation in Bacopa monnieri. International Journal of Biological Sciences, 13(4), 369-377.
Coste, A., Vlase, L., Halmagyi, A., Deliu, C. & Coldea, G. (2011). Effects of plant growth regulators and elicitors on production of secondary metabolites in shoot cultures of Hypericum hirsutum and Hypericum maculatum. Plant Cell, Tissue and Organ Culture, 106, 279-288.
Gadzovska, S., Maury, S., Delaunay, A. & et al. (2013). The influence of salicylic acid elicitation of shoots, callus, and cell suspension cultures on production of naphtodianthrones and phenylpropanoids in Hypericum perforatum L. Plant Cell, Tissue and Organ Culture,113, 25–39. https://doi.org/10.1007/s11240-012-0248-0.
Galeotti, N. (2017). Hypericum perforatum (St John’s wort) beyond depression: A therapeutic perspective for pain conditions. Journal of Ethnopharmacology, 200, 136–146.
Greeson, J.M., Sanford, B., & Monti, D.A. (2001). St. John’s wort (Hypericum perforatum): a review of the current pharmacological, toxicological, and clinical literature. Psychopharmacology, 153, 402–414. doi: 10.1007/s002130000625.
Grover, J.K., Yadav, S., & Vats, V. (2002). Medicinal plants of India with anti-diabetic potential. Journal of Ethnopharmacology, 81, 81–100.
Humbal, A., & Pathak, B. (2023) Influence of exogenous elicitors on the production of secondary metabolite in plants: A review (“VSI: secondary metabolites”), Plant Stress, 8,100166,
Halder, M., Sarkar, S., & Jha, S. (2019). Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Engineering in Life Sciences, 19, 880.
Jeyasri, R., Muthuramalingam, P., Karthick, K.  & et al. (2023). Methyl jasmonate and salicylic acid as powerful elicitors for enhancing the production of secondary metabolites in medicinal plants: an updated review. Plant Cell, Tissue and Organ Culture, 153, 447–458. https://doi.org/10.1007/s11240-023-02485-8.
Kandoudi, W., Radácsi, P., Gosztola, B., Zámborine Németh, E. (2021). Elicitation of medicinal plants in vivo—Is it a realistic tool? The effect of methyl jasmonate and salicylic acid on lamiaceae species. Horticulturae, 8(1), 5: https://doi.org/10.3390/horticulturae8010005.
Kenda, M., Kočevar Glavač, N., Nagy, M., & Sollner Dolenc, M. (2022). Medicinal plants used for anxiety, depression, or stress treatment: An update. Molecules 15;27(18):6021. doi: 10.3390/molecules27186021.
Khan, S.A., Verma, P., & Parasharami, V.A. (2022). RETRACTED ARTICLE: Homo and heterologous expression of the HpPKS2 gene in Hypericum perforatum and Bacopa monnieri. Plant Cell, Tissue and Organ Culture, 148, 215. https://doi.org/10.1007/s11240-020-01965-5.
Kianersi, F., Amin Azarm, D., Fatemi, F., Jamshidi, B., Pour-Aboughadareh, A., Janda, T. (2023). The influence of methyl jasmonate on expression patterns of rosmarinic acid biosynthesis genes, and phenolic compounds in different Species of Salvia subg. Perovskia Kar L. Genes, 5, 14(4):871. doi: 10.3390/genes14040871.
Klingauf, P., Beuerle, T., Mellenthin, A., El-Moghazy, S.A., Boubakir, Z., & Beerhues, L. (2005). Biosynthesis of the hyperforin skeleton in Hypericum calycinum cell cultures. Phytochemistry, 66, 139-145.
Kumari, R., &Kotecha, M. (2016) A review on the standardization of herbal medicines. International Journal of Pharmaceutical Sciences, 7(2), 97–106.
Largia, M.J.V., Pothiraj, G., Shilpha, J., Ramesh, M. (2015). Methyl jasmonate and salicylic acid synergism enhances bacoside A content in shoot cultures of Bacopa monnieri (L). Plant Cell, Tissue and Organ Culture, 122(1), 9–20.
Linde, K., Ramirez, G., Mulrow, C.D., Pauls, A., Weidenhammer, W., & Melchart, D. (1996). St. John's wort for depression.  British Medical Journal, 313, 253-258.
Mazzara, M., & James, D.J. (2000). The influence of photoperiodic growth condition on isolation of RNA from strawberry (Fragaria× ananassa Duch.) tissue. Molecular biotechnology, 15, 237-241.
Miladinova-Georgieva, K., Geneva, M., Stancheva, I., Petrova, M., Sichanova, M., & Kirova, E. (2022). Effects of different elicitors on micropropagation, biomass and secondary metabolite production of Stevia rebaudiana Bertoni.—A Review. Plants12, 153. https://doi.org/10.3390/plants12010153.
Mozaffarian, V. (2015). Identification of Medicinal and Aromatic Plants of Iran. Farhang Moaser Publishers, 1444 p. (In Persian).
Oksman-Caldentey, K.-M. and Inzé, D. 2004. Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends in plant science, 9: 433-440.
Omidbeygi, R. (2000). Approaches Production and Processing of Medicinal Plants. Fekre Rooz Publishers, 242 p. (In Persian).
Patocka, J. (2003). The chemistry, pharmacology, and toxicology of the biologically active constituents of the herb Hypericum perforatum L. Journal of Applied Biomedicine, 1, 61–70.
Pradeep, M., & Franklin, G. (2022). Understanding the hypericin biosynthesis via reversible inhibition of dark gland development in Hypericum perforatum L. Industrial Crops and Products, 182,114876,
Qin, X., Venkatanarayanan, N., & Yih Xian Ho, C. (2017). Clinical use of Hypericum perforatum (St John's wort) in depression: A meta-analysis. Journal of Affective Disorders, 210, 211-221, https://doi.org/10.1016/j.jad.2016.12.048.
Rattan, S., & Warghat Ashish., R. (2023). Comparative analysis of salidroside and rosavin accumulation and expression analysis of biosynthetic genes in salicylic acid and methyl jasmonate elicited cell suspension culture of Rhodiola imbricata (Edgew.). Industrial Crops and Products, 198, 2023,116667,
Saeed, S., Ali, H., Khan, T., Kayani, W., & Khan, M.A. (2017). Impacts of methyl jasmonate and phenyl acetic acid on biomass accumulation and antioxidant potential in adventitious roots of Ajuga bracteosa Wall ex Benth., a high valued endangered medicinal plant. Physiology and  Molocular Biology of Plants, 23, 229–237.
Sharma, M., Ahuja, A., Gupta, R., & Mallubhotla, S. (2015) Enhanced bacoside production in shoot cultures of Bacopa monnieri under the influence of abiotic elicitors. Natural Product Research, 29, 745–749.
Sirvent, T., Gibson, D. (2002). Induction of hypericins and hyperforin in Hypericum perforatum L. in response to biotic and chemical elicitors. Physiological and Molecular Plant Pathology, 60, 311-320.
Sirvent. T, Krasnoff, S.B., Gibson, D. (2003). Induction of hypericins and hyperforins in Hypericum perforatum in response to damage by herbivores. Journal of Chemical Ecology, 29(12), 2667-81.
Soták, M., Czeranková, O., Klein, D., Jurčacková, Z., Li, L., & Čellárová, E. (2016). Comparative transcriptome reconstruction of four Hypericum species focused on hypericin biosynthesis. Frontiers in Plant Sciences, 7,1039. doi: 10.3389/fpls.2016.01039.
Su, H., Li, J., Chen, S., Sun, P., Xing, H., Yang, D., Zhang, X., Li, M., & Wei, J. (2021). Physiological and transcriptomic analysis provide insight into low temperature enhancing hypericin biosynthesis in Hypericum perforatumMolecules, 26(8), 2294. https://doi.org/10.3390/molecules26082294.
Tang, H., Hu, J., Zhao, M., & et al. (2023). Comparative study of the physiological responses, secondary metabolites, and gene expression of medicinal plant Prunella vulgaris L. treated with exogenous methyl jasmonate and salicylic acid. Acta Physiol Plant45, 20. https://doi.org/10.1007/s11738-022-03498-0.
Volz, H.P. (2022). Hypericum and depression. In: Riederer, P., Laux, G., Nagatsu, T., Le, W., & Riederer, C. (eds) NeuroPsychopharmacotherapy. Springer, Cham. https://doi.org/10.1007/978-3-030-62059-2_93.
Vuko, E., Dunkić, V., Ruščić, M., Nazlić, M., Mandić, N., Soldo, B., Šprung, M., Fredotović, Ž. (2021). Chemical composition and new biological activities of essential oil and hydrosol of Hypericum perforatum L. ssp. veronense (Schrank) H. Lindb. Plants. 10(5):1014. https://doi.org/10.3390/plants10051014.
Walker, T.S., Bais, H.P., & Vivanco, J.M. (2002). Jasmonic acid-induced hypericin production in cell suspension cultures of Hypericum perforatum L. (St. John's wort). Phytochemistry, 60, 289-293.
Waranya, B., Sujipuli, K., & Prasarnpun, S. (2018). Effect of methyl jasmonate elicitation on biomass, gene expression and saponin accumulation in Bacopa monnieri. International Journal of Biosciences, 13 (4), 369-377. http://dx.doi.org/10.12692/ijb/13.4.369-377.
Wurglics, M., & Schubert-Zsilavecz, M. (2006). Hypericum perforatum: a ‘modern’ herbal antidepressant: pharmacokinetics of active ingredients. Clinical Pharmacokinetics, 45, 449–468. doi: 10.2165/00003088-200645050-00002.
Zamani, M., Moradi, H., Vida Chalavi, V., Kazemitabar, S.K. (2019). Effect of salicylic asid and methyle jasmonat elicitors on hypericin production in stJohn’s wort (Hypericum perforatum L.) cv. topas callus culture. Iranian Journal of Horticultural Science , 49(4), 915-923. (In Persian).
Zhou, W., Wang, S., Yang, L., Sun, Y., Zhang, Q., Li, B., Wang, B., Li, L., Wang, D., & Wang, Z. (2019). Reference genes for qRT-PCR normalisation in different tissues, developmental stages, and stress conditions of Hypericum perforatumPeerJ7, e7133. doi: 10.7717/peerj.7133.