Methyl jasmonate enhances the anti-inflammatory effects of the adventitious roots in Abeliophyllum distichum by increasing the production of polyphenolic compounds

  • T.K. Hyun Department of Industrial Plant Science and Technology
  • S.G. Bang
  • M.-A. Ahn
  • S.H. Eom
  • W.T. Joeng
Keywords: Abeliophyllum distichum, Adventitious root, Anti-inflammatory effect, Methyl jasmonate

Abstract

Abeliophyllum distichum has been demonstrated to possess anticancer, anti-inflammatory, anti-osteoporotic, and anti-obesity effects. However, there is a limitation to using this shrub as a beneficial material, because this shrub had been listed as endangered. Thus, we established an adventitious root culture of A. distichum (AdAR) to overcome this limitation. Solvent-solvent partition fractions from methanol extract of methyl jasmonate (MeJA)-elicited AdAR were used, and the ethyl acetate fraction of MeJA-treated AdAR (EtOAc/MeJA) exhibited strong anti-inflammatory effects in lipopolysaccharide (LPS)-treated RAW264.7 cells. EtOAc/MeJA downregulated the transcription of pro-inflammatory genes and mediators by inhibiting the LPS-activated MEK/ERK signaling pathway. In addition, the results of the phytochemical analysis suggested that MeJA induced the accumulation of polyphenolic compounds, including p-coumaric and ferulic acids, by inducing phenylpropanoid biosynthetic genes in AdAR. These results suggested that AdAR is a viable source for overcoming limitations in the industrial use of A. distichum.

References

Alarcón, M.V., Salguero, J. and Lloret, P.G. (2019) Auxin modulated initiation of lateral roots is linked to pericycle cell length in maize. Frontiers in Plant Science 10, 11. https://doi.org/10.3389/fpls.2019.00011.

Albarrán-Mondragón, F.J., Orozco-Villafuerte, J., Mulia-Rodriguez, J., Hernández-Jaimes, C., Cruz-Sosa, F. and Buendía-González. L. (2022). Total phenolic content in fruits and in in vitro cultures of Bromelia karatas L. Revista Mexicana de Ingeniería Química 21, Bio2685. https://doi.org/10.24275/rmiq/Bio2685.

Barbez, E., Dünser, K., Gaidora, A., Lendl, T. and Busch, W. (2017). Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 114, E4884–E4893. https://doi.org/10.1073/pnas.1613499114.

Chang, C.F., Liao, K.C. and Chen, C.H. (2017). 2-Phenylnaphthalene derivatives inhibit lipopolysaccharide-induced pro-inflammatory mediators by downregulating of MAPK/NF-κB pathways in RAW 264.7 macrophage cells. PLoS One 12, e0168945. https://doi.org/10.1371/journal.pone.0168945.

Choi, J.H., Seo, E.-J., Sung, J., Choi, K.M., Kim, H., Kim, J.-S., Lee, J., Efferth, T. and Hyun, T.K. (2017). Polyphenolic compounds, antioxidant and anti-inflammatory effects of Abeliophyllum distichum Nakai extract. Journal of Applied Botany and Food Quality 90, 266–273. https://doi.org/10.5073/JABFQ.2017.090.033.

Choi, J.H., Kim, H. and Hyun, T.K. (2018). Transcriptome analysis of Abeliophyllum distichum NAKAI reveals potential molecular markers and candidate genes involved in anthocyanin biosynthesis pathway. South African Journal of Botany 116, 34–41. https://doi.org/10.1016/j.sajb.2018.02.401.

Cocetta, G., Rossoni, M., Gardana, C., Mignani, I., Ferrante, A. and Spinardi, A. (2015). Methyl jasmonate affects phenolic metabolism and gene expression in blueberry (Vaccinium corymbosum). Physiologia Plantarum 153, 269–283. https://doi.org/10.1111/ppl.12243.

Deepthi, S. and Satheeshkumar, K., (2017). Effects of major nutrients, growth regulators and inoculum size on enhanced growth and camptothecin production in adventitious root cultures of Ophiorrhiza mungos L. Biochemical Engineering Journal 117, 198–209. https://doi.org/10.1016/j.bej.2016.10.016.

Eom, J., Thomas, S.S., Sung, N.Y., Kim, D.S., Cha, Y.S. and Kim, K.A. (2020). Abeliophyllum distichum ameliorates high-fat diet-induced obesity in C57BL/6J mice by upregulating the AMPK Pathway. Nutrients 12, 3320. https://doi.org/10.3390/nu12113320.

Ghimire, B. and Heo, K. (2014). Embryology of Abeliophyllum (Oleaceae) and its phylogenetic relationships. Nordic Journal of Botany 32, 632–641. https://doi.org/10.1111/j.1756-1051.2013.00204.x.

Guha, M. and Mackman, N. (2001). LPS induction of gene expression in human monocytes. Cellular Signalling 13, 85–94. https://doi.org/10.1016/s0898-6568(00)00149-2.

Halder, M., Sarkar, S. and Jha, S. (2019). Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Engineering in Life Sciences 19, 880–895. https://doi.org/10.1002/elsc.201900058.

Hussain, M.J., Abbas, Y., Nazli, N., Fatima, S., Drouet, S., Hano, C. and Abbasi, B.H. (2022). Root cultures, a boon for the production of valuable compounds: a comparative review. Plants 11, 439. https://doi.org/10.3390/plants11030439.

Jin, S., Kim, K.C., Kim, J.S., Jang, K.I. and Hyun, T.K. (2020). Anti-melanoma activities and phytochemical compositions of Sorbus commixta fruit extracts. Plants 9, 1076. https://doi.org/10.3390/plants9091076.

Ju, H.J., Kim, K.C., Kim, H., Kim, J.-S. and Hyun, T.K. (2021a). Variability of polyphenolic compounds and biological activities among Perilla frutescens var. crispa genotypes. Horticulturae 7, 404. https://doi.org/10.3390/horticulturae7100404.

Ju, H.J., Lim, H.B. and Hyun, T.K. (2021b). The chemical composition and anti-inflammatory effect of the essential oil obtained from Abeliophyllum distichum flowers. Botanica Serbica 45, 137–142. https://doi.org/10.2298/BOTSERB2101137J.

Kaminska, B. (2005). MAPK signalling pathways as molecular targets for anti-inflammatory therapy--from molecular mechanisms to therapeutic benefits. Biochimica et Biophysica Acta 1754, 253–262. https://doi.org/10.1016/j.bbapap.2005.08.017.

Khanam, M.N., Anis, M., Javed, S.B., Mottaghipisheh, J. and Csupor, D. (2022). Adventitious root culture-an alternative strategy for secondary metabolite production: a review. Agronomy 12, 1178. https://doi.org/10.3390/agronomy12051178.

Kim, D.S., Um, Y.R. and Ma, J.Y. (2014). Flavonoid content, free radical scavenging and increase in xanthine oxidase inhibitory activity in Galgeun-tang following fermentation with Lactobacillus plantarum. Molecular Medicine Reports 10, 2689–2693. https://doi.org/10.3892/mmr.2014.2487.

Kim, E., Mok, H.K. and Hyun, T.K. (2022). Variations in the antioxidant, anticancer, and anti-inflammatory properties of different Rosa rugosa organ extracts. Agronomy 12, 238. https://doi.org/10.3390/agronomy12020238.

Kim, N.Y. and Lee, H.Y. (2015). Enhancement of anti-wrinkle activities of Abeliophyllum distichum Nakai through low temperature extraction process. Korean Journal of Medicinal Crop Science 23, 231–236. ISSN:1225-9306.

Kreis, W. (2019). Exploiting plant cell culture for natural product formation. Journal of Applied Botany and Food Quality 92, 216–225. https://doi.org/10.5073/JABFQ.2019.092.030.

Lee, J.K., Eom, S.H. and Hyun, T.K. (2018). Enhanced biosynthesis of saponins by coronatine in cell suspension culture of Kalopanax septemlobus. 3 Biotech 8, 59. https://doi.org/10.1007/s13205-018-1090-9.

Lee, J.-H., Ong, H.G., Kim, B.-Y., Kim, Y.-I., Jung, E.-K., Chung, M.G. and Kim, Y.-D. (2022). Population genomics study for the conservation management of the endangered shrub Abeliophyllum distichum. Conservation Genetics. https://doi.org/10.1007/s10592-022-01447-5.

Lee, K., Jang, Y.J., Lee, H., Kim, E., Kim, Y., Yoo, T.K., Hyun, T.K., Park, J.I., Yi, S.J. and Kim, K. (2020). Transcriptome analysis reveals that Abeliophyllum distichum Nakai extract inhibits RANKL-mediated osteoclastogenensis mainly through suppressing Nfatc1 expression. Biology 9, 212. https://doi.org/10.3390/biology9080212.

Li, J., Li, B., Luo, L., Cao, F., Yang, B., Gao, J., Yan, Y., Zhang, G., Peng, L. and Hu, B. (2020). Increased phenolic acid and tanshinone production and transcriptional responses of biosynthetic genes in hairy root cultures of Salvia przewalskii Maxim. treated with methyl jasmonate and salicylic acid. Molecular Biology Reports 47, 8565–8578. https://doi.org/10.1007/s11033-020-05899-1.

Loh, K.E., Chin, Y.S., Safinar Ismail, I. and Tan, H.Y. (2022). Rapid characterisation of xanthine oxidase inhibitors from the flowers of Chrysanthemum morifolium Ramat. Using metabolomics approach. Phytochemical Analysis 33, 12–22. https://doi.org/10.1002/pca.3057.

López-Ramírez, Y., Cabañas-García, E., Areche, C., Trejo-Tapia, G., Pérez-Molphe-Balch, E. and Gómez-Aguirre, Y.A. (2021) Callus induction and phytochemical profiling of Yucca carnerosana (Trel.) McKelvey obtained from in vitro cultures. Revista Mexicana de Ingeniería Química 20, 823–387. https://doi.org/10.24275/rmiq/Bio2209.

Lu, X. and Hyun, T.K. (2021). Histone deacetylase inhibitors improve MeJA-induced ginsenoside production in ginseng adventitious roots. Industrial Crops and Products 171, 113909. https://doi.org/10.1016/j.indcrop.2021.113909.

Moon, H.K., Suk, G.Y., Kwon, Y.J. and Son, S.H. (1999). Micropropagation of a rare species, Abeliophyllum distichum Nakai. via axillary bud culture. Korean Journal of Plant Tissue Culture 26, 133–136. https://doi.org/10.1016/1872-2075(08)60035-7.

Murthy, H.N., Hahn, E.J. and Paek, K.Y. (2008). Adventitious roots and secondary metabolism. Shengwu Gongcheng Xuebao 24, 711–716.

Ochoa-Villarreal, M., Howat, S., Hong, S., Jang, M.O., Jin, Y.W., Lee, E.K. and Loake, G.J. (2016). Plant cell culture strategies for the production of natural products. BMB Reports 49, 149-158. https://doi.org/10.5483/bmbrep.2016.49.3.264.

Oh, H., Kang, D.G., Kwon, T.O., Jang, K.K., Chai, K.Y., Yun, Y.G., Chung, H.T. and Lee, H.S. (2003). Four glycosides from the leaves of Abeliophyllum distichum with inhibitory effects on angiotensin converting enzyme. Phytotherapy Research 17, 811–813. https://doi.org/10.1002/ptr.1199.

Qin, S., Liu, Y., Yan, J., Lin, S., Zhang, W. and Wang, B. (2022). An optimized tobacco hairy root induction system for functional analysis of nicotine biosynthesis-related genes. Agronomy 12, 348. https://doi.org/10.3390/agronomy12020348.

Sengar, R.S., Chaudhary R. and Tyagi S.K. (2010). Present status and scope of floriculture developed through different biological tools. Research Journal of Agricultural Science 14306314.

Tao, X., Wu, Q., Li, J., Huang, S., Cai, L., Mao, L., Luo, Z., Li, L. and Ying, T. (2022). Exogenous methyl jasmonate regulates phenolic compounds biosynthesis during postharvest tomato ripening. Postharvest Biology and Technology 184, 111760. https://doi.org/10.1016/j.postharvbio.2021.111760.

Tinco-Jayo, J.A., Aguilar-Felices, E.J., Enciso-Roca, E.C., Arroyo-Acevedo, J.L. and Herrera-Calderon, O. (2021). Phytochemical screening by LC-ESI-MS/MS and effect of the ethyl acetate fraction from leaves and stems of Jatropha macrantha Müll Arg. on ketamine-induced erectile dysfunction in rats. Molecules 27, 115. https://doi.org/10.3390/molecules27010115.

Wang, J., Man, S., Gao, W., Zhang, L. and Huang, L. (2013). Cluster analysis of ginseng tissue cultures, dynamic change of growth, total saponins, specific oxygen uptake rate in bioreactor and immuno-regulative effect of ginseng adventitious root. Industrial Crops and Products 41, 57–63. https://doi.org/10.1016/j.indcrop.2012.04.005.

Wu, T., Kerbler, S.M., Fernie, A.R. and Zhang, Y. (2021). Plant cell cultures as heterologous bio-factories for secondary metabolite production. Plant Communications 2, 100235. https://doi.org/10.1016/j.xplc.2021.100235.

Xing, B., Yang, D., Liu, L., Han, R., Sun, Y. and Liang, Z. (2018). Phenolic acid production is more effectively enhanced than tanshinone production by methyl jasmonate in Salvia miltiorrhiza hairy roots. Plant Cell, Tissue and Organ Culture 134, 119–129. https://doi.org/10.1007/s11240-018-1405-x.

Yi, T.G., Park, Y., Park, J.-E. and Park, N.I. (2019). Enhancement of phenolic compounds and antioxidative activities by the combination of culture medium and methyl jasmonate elicitation in hairy root cultures of Lactuca indica L. Natural Product Communications 14, 1–9. https://doi.org/10.1177/1934578X19861867.

Yin, P., Zhang, Z., Li, J., Shi, Y., Jin, N., Zou, W., Gao, Q., Wang, W. and Liu, F. (2019). Ferulic acid inhibits bovine endometrial epithelial cells against LPS-induced inflammation via suppressing NK-κB and MAPK pathway. Research in Veterinary Science 126, 164–169. https://doi.org/10.1016/j.rvsc.2019.08.018.

Yoo, T.K., Jeong, W.T., Kim, J.G., Ji, H.S., Ahn, M.A., Chung, J.W., Lim, H.B. and Hyun, T.K. (2021). UPLC-ESI-Q-TOF-MS-based metabolite profiling, antioxidant and anti-inflammatory properties of different organ extracts of Abeliophyllum distichum. Antioxidants 10, 70. https://doi.org/10.3390/antiox10010070.

Yoo, T.K., Kim, J.S. and Hyun, T.K. (2020). Polyphenolic composition and anti-melanoma activity of white forsythia (Abeliophyllum distichum Nakai) organ extracts. Plants 9, 757. https://doi.org/10.3390/plants9060757.

Yue, W., Ming, Q.L., Lin, B., Rahman, K., Zheng, C.J., Han, T. and Qin, L.P. (2016). Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Critical Reviews in Biotechnology 36, 215–232. https://doi.org/10.3109/07388551.2014.923986.

Zhao, Y., Liu, J., Liu, C., Zeng, X., Li, X. and Zhao, J. (2016). Anti-inflammatory effects of p-coumaric acid in LPS-Stimulated RAW264.7 cells: Involvement of NF-κB and MAPKs pathways. Medicinal Chemistry 6, 327–330. https://doi.org/ 10.4172/2161-0444.1000365.

Zhou, W., Shi, M., Deng, C., Lu, S., Huang, F., Wang, Y. and Kai, G. (2021). The methyl jasmonate-responsive transcription factor SmMYB1 promotes phenolic acid biosynthesis in Salvia miltiorrhiza. Horticulture Research 8, 10. https://doi.org/10.1038/s41438-020-00443-5.

Published
2022-07-11
How to Cite
Hyun, T., Bang, S., Ahn, M.-A., Eom, S., & Joeng, W. (2022). Methyl jasmonate enhances the anti-inflammatory effects of the adventitious roots in Abeliophyllum distichum by increasing the production of polyphenolic compounds. Revista Mexicana De Ingeniería Química, 21(2), Bio2819. https://doi.org/10.24275/rmiq/Bio2819
Section
Biotechnology