Methyl Jasmonate Elicitation Enhanced Biomass, Phenolic, and Flavonoid Production of Adventitious Root Culture of Gynura procumbens in Balloon Type Bubble Bioreactor

https://doi.org/10.22146/mot.87736

Ely Tri Wijayanti(1), Dannis Yuda Kusuma(2), Alfinda Novi Kristanti(3), Anjar Tri Wibowo(4), Sugiharto Sugiharto(5), Djarot Sugiarso(6), Yosephine Sri Wulan Manuhara(7*)

(1) Department of Biology, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(2) Department of Biology, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(3) Department of Chemistry, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(4) Department of Biology, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(5) Department of Biology, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(6) Department of Analytic, Faculty of Science and Analytical Data, Institut Teknologi Sepuluh Nopember, Surabaya, East Java
(7) Department of Biology, Faculty of Science and Technology, Universitas Airlangga, Surabaya, East Java
(*) Corresponding Author

Abstract


Secondary metabolites in the medicinal plant Gynura procumbens have various beneficial pharmacological activities. However, the limited availability of these beneficial compounds has constrained the possibilities for therapeutic applications. Exogenously applied methyl jasmonate (MeJa) as an elicitor has been reported to trigger the accumulation of secondary metabolites in plant tissues cultured in vitro. This study aimed to assess how varying periods of MeJa elicitation affect the growth and accumulation of phenolic and flavonoid compounds in adventitious root cultures of G. procumbens within a balloon-type bubble bioreactor (BTBB). Adventitious roots were induced from leaf and stem explants obtained from established in vitro shoots. Upon transfer to the BTBB, the cultures were supplemented with 100 µM MeJa and sampled at 1, 2, 3, and 4 weeks. The results revealed that including MeJa in the culture medium significantly boosted growth and the accumulation of phenolic and flavonoid compounds in G. procumbens. The highest biomass and concentrations of phenolic and flavonoid compounds were observed after 3 weeks of elicitation. These findings highlight the potential of MeJa elicitation for enhancing the production of valuable bioactive compounds in G. procumbens adventitious root cultures, showcasing its utility for industrial applications.


Keywords


balloon-type bubble bioreactor; flavonoid; Gynura procumbens; methyl jasmonate; phenol

Full Text:

PDF


References

Algariri, K., Meng, K. Y., Atangwho, I. J., Asmawi, M. Z., Sadikun, A., Murugaiyah, V., & Ismail, N. (2013). Hypoglycemic and anti–hyperglycemic study of Gynura procumbens leaf extracts. Asian Pacific Journal of Tropical Biomedicine, 3(5), 358–366. https://doi.org/10.1016/S2221-1691(13)60077-5

Ali, M., Hahn, E.-J., & Paek, K.-Y. (2007). Methyl Jasmonate and Salicylic Acid Induced Oxidative Stress and Accumulation of Phenolics in Panax ginseng Bioreactor Root Suspension Cultures. Molecules, 12(3), 607–621. https://doi.org/10.3390/12030607

Anwar Hossain, M., Hoque, M. A., Burritt, D. J., & Fujita, M. (2014). Proline Protects Plants Against Abiotic Oxidative Stress: Biochemical and Molecular Mechanisms. In Oxidative Damage to Plants: Antioxidant Networks and Signaling (pp. 477–522). Elsevier Inc. https://doi.org/10.1016/B978-0-12-799963-0.00016-2

Baque, A., Murthy, H. N., & Paek, K.-Y. (2014). Adventitious Root Culture of Morinda citrifolia in Bioreactors for Production of Bioactive Compounds. In Production of Biomass and Bioactive Compounds Using Bioreactor Technology (pp. 185–222). Springer Netherlands. https://doi.org/10.1007/978-94-017-9223-3_9

Baque, Md. A., Shiragi, Md. H. K., Moh, S.-H., Lee, E.-J., & Paek, K.-Y. (2013). Production of biomass and bioactive compounds by adventitious root suspension cultures of Morinda citrifolia (L.) in a liquid-phase airlift balloon-type bioreactor. In Vitro Cellular & Developmental Biology - Plant, 49(6), 737–749. https://doi.org/10.1007/s11627-013-9555-3

Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207. https://doi.org/10.1007/BF00018060

Choi, S. M., Ho Son, S., Rho Yun, S., Woung Kwon, O., Hoon Seon, J., & Yoeup Paek, K. (2000). Pilot-Scale Culture of Adventitious Roots of Ginseng in a Bioreactor System. Plant Cell, Tissue and Organ Culture, 62(3), 187–193. https://doi.org/10.1023/A:1006412203197

Cui, X.-H., Chakrabarty, D., Lee, E.-J., & Paek, K.-Y. (2010). Production of adventitious roots and secondary metabolites by Hypericum perforatum L. in a bioreactor. Bioresource Technology, 101(12), 4708–4716. https://doi.org/10.1016/j.biortech.2010.01.115

Davey, M. W., Stals, E., Panis, B., Keulemans, J., & Swennen, R. L. (2005). High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry, 347(2), 201–207. https://doi.org/10.1016/j.ab.2005.09.041

Dewir, Y. H., Chakrabarty, D., Ali, M. B., Hahn, E. J., & Paek, K. Y. (2005). Effects of Hydroponic Solution EC, Substrates, PPF and Nutrient Scheduling on Growth and Photosynthetic Competence During Acclimatization of Micropropagated Spathiphyllum plantlets. Plant Growth Regulation, 46(3), 241–251. https://doi.org/10.1007/s10725-005-0161-1

Esfandiari, E., Shekari, F., Shekari, F., & Esfandiari, M. (2007). The effect of salt stress on antioxidant enzymes activity and lipid peroxidation on the wheat seedling. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 35(1), 48–56.

Faizah, H., Tanjung, M., Purnobasuki, H., & Manuhara, Y. S. W. (2018). Biomass and flavonoid production of Gynura procumbens (L.). merr adventitious root culture in baloon-type bubble-bioreactor influenced by elicitation. Asian Journal of Plant Sciences, 17(2), 107–119. https://doi.org/10.3923/AJPS.2018.107.119

Foyer, C. H., & Harbinson, J. (2019). Oxygen Metabolism and the Regulation of Photosynthetic Electron Transport. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants (pp. 1–42). CRC Press. https://doi.org/10.1201/9781351070454-1

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(3), 716. https://doi.org/10.3390/ijms21030716

Hoe, S.-Z., Lee, C.-N., Mok, S.-L., Kamaruddin, M. Y., & Lam, S.-K. (2011). Gynura procumbens Merr. decreases blood pressure in rats by vasodilatation via inhibition of calcium channels. Clinics, 66(1), 143–150. https://doi.org/10.1590/S1807-59322011000100025

Iskander, M. N., Song, Y., Coupar, I. M., & Jiratchariyakul, W. (2002). Antiinflammatory screening of the medicinal plant Gynura procumbens. Plant Foods for Human Nutrition, 57(3/4), 233–244. https://doi.org/10.1023/A:1021851230890

Jarikasem, S., Charuwichitratana, S., Siritantikorn, S., Chantratita, W., Iskander, M., Frahm, A. W., & Jiratchariyakul, W. (2013). Antiherpetic Effects of Gynura procumbens. Evidence-Based Complementary and Alternative Medicine, 2013, 1–10. https://doi.org/10.1155/2013/394865

Jiang, X.-L., Piao, X.-C., Ri Gao, Jin, M.-Y., Jiang, J., Jin, X.-H., & Lian, M.-L. (2017). Improvement of bioactive compound accumulation in adventitious root cultures of an endangered plant species, Oplopanax elatus. Acta Physiologiae Plantarum, 39(10), 226. https://doi.org/10.1007/s11738-017-2525-3

Jiao, C., Song, C., Zheng, S., Zhu, Y., Jin, Q., Cai, Y., & Lin, Y. (2018). Metabolic Profiling of Dendrobium officinale in Response to Precursors and Methyl Jasmonate. International Journal of Molecular Sciences, 19(3), 728. https://doi.org/10.3390/ijms19030728

Kaewseejan, N., Sutthikhum, V., & Siriamornpun, S. (2015). Potential of Gynura procumbens leaves as source of flavonoid-enriched fractions with enhanced antioxidant capacity. Journal of Functional Foods, 12, 120–128. https://doi.org/10.1016/j.jff.2014.11.001

Karuppusamy, S. (2009). A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. In Journal of Medicinal Plants Research (13th ed., Vol. 3, pp. 1222–1239).

Kavi Kishor, P. B. (2015). Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Frontiers in Plant Science, 6. https://doi.org/10.3389/fpls.2015.00544

Kim, J., Lee, C.-W., Kim, E. K., Lee, S.-J., Park, N.-H., Kim, H.-S., Kim, H.-K., Char, K., Jang, Y. P., & Kim, J.-W. (2011). Inhibition effect of Gynura procumbens extract on UV-B-induced matrix-metalloproteinase expression in human dermal fibroblasts. Journal of Ethnopharmacology, 137(1), 427–433. https://doi.org/10.1016/j.jep.2011.04.072

Kim, Y., Hahn, E., Murthy, H. N., & Paek, K. (2004). Adventitious root growth and ginsenoside accumulation in Panax ginseng cultures as affected by methyl jasmonate. Biotechnology Letters, 26(21), 1619–1622. https://doi.org/10.1007/s10529-004-3183-2

Kochan, E., Szymczyk, P., Kuźma, Ł., Szymańska, G., Wajs-Bonikowska, A., Bonikowski, R., & Sienkiewicz, M. (2018). The Increase of Triterpene Saponin Production Induced by Trans-Anethole in Hairy Root Cultures of Panax quinquefolium. Molecules, 23(10), 2674. https://doi.org/10.3390/molecules23102674

Krishnan, V., Ahmad, S., & Mahmood, M. (2015). Antioxidant Potential in Different Parts and Callus of Gynura procumbens and Different Parts of Gynura bicolor. BioMed Research International, 2015, 1–7. https://doi.org/10.1155/2015/147909

Lee, E. J., Park, S. Y., & Paek, K. Y. (2015). Enhancement strategies of bioactive compound production in adventitious root cultures of Eleutherococcus koreanum Nakai subjected to methyl jasmonate and salicylic acid elicitation through airlift bioreactors. Plant Cell, Tissue and Organ Culture (PCTOC), 120(1), 1–10. https://doi.org/10.1007/s11240-014-0567-4

Lee, E.-J., Moh, S.-H., & Park, S.-Y. (2014). Production of Biomass and Bioactive Compounds in Adventitious Root Cultures of Eleutherococcus koreanum Nakai. In Production of Biomass and Bioactive Compounds Using Bioreactor Technology (pp. 223–249). Springer Netherlands. https://doi.org/10.1007/978-94-017-9223-3_10

Lee, E.-J., & Paek, K.-Y. (2012). Effect of nitrogen source on biomass and bioactive compound production in submerged cultures of Eleutherococcus koreanum nakai adventitious roots. Biotechnology Progress, 28(2), 508–514. https://doi.org/10.1002/btpr.1506

Mangas, S., Bonfill, M., Osuna, L., Moyano, E., Tortoriello, J., Cusido, R. M., Teresa Piñol, M., & Palazón, J. (2006). The effect of methyl jasmonate on triterpene and sterol metabolisms of Centella asiatica, Ruscus aculeatus and Galphimia glauca cultured plants. Phytochemistry, 67(18), 2041–2049. https://doi.org/10.1016/j.phytochem.2006.06.025

Manogaran, M., Lim, V., & Mohamed, R. (2019). Phytoconstituents of the Gynura procumbens ethanol leaf extract and its fractions and their effects on viability of macrophages. Journal of Herbmed Pharmacology, 8(3), 224–230. https://doi.org/10.15171/jhp.2019.33

Manuhara, Y. S. W., Kusuma, D. Y., Sari, R. L. K., & Kristanti, A. N. (2017). Biomass Production of Gynura procumbens Adventitious Roots in Different Type of Liquid Culture. Biosaintifika: Journal of Biology & Biology Education, 9(3), 523–529. https://doi.org/10.15294/biosaintifika.v9i3.9670

Matter, M. A., Hanafy, M. S., & Aly, U. I. (2017). Effect of Methyl Jasmonate and Mannitol Application on Growth and Eugenol Content in Callus Cultures of Carnation. Plant Tissue Culture and Biotechnology, 27(2), 227–240. https://doi.org/10.3329/ptcb.v27i2.35028

Mendoza, D., Cuaspud, O., Arias, 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

Miyanaga, K., Seki, M., & Furusaki, S. (2000). Quantitative determination of cultured strawberry-cell heterogeneity by image analysis: effects of medium modification on anthocyanin accumulation. Biochemical Engineering Journal, 5(3), 201–207. https://doi.org/10.1016/S1369-703X(00)00059-0

Murthy, H. N., Dandin, V. S., & Paek, K.-Y. (2016). Tools for biotechnological production of useful phytochemicals from adventitious root cultures. Phytochemistry Reviews, 15(1), 129–145. https://doi.org/10.1007/s11101-014-9391-z

Muthoharoh, L., Faizah, H., Hartatie Hardjo, P., Novi Kristanti, A., & Sri Wulan Manuhara, Y. (2019). Effect of Carbon Source on Biomass and Flavonoid Content of Gynuraprocumbens (Lour.) Merr Adventitious Root in Liquid Culture. Biosciences, Biotechnology Research Asia, 16(1), 121–127. https://doi.org/10.13005/bbra/2729

Ng, H.-K., Poh, T.-F., Lam, S.-K., & Hoe, S.-Z. (2013). Potassium channel openers and prostacyclin play a crucial role in mediating the vasorelaxant activity of Gynura procumbens. BMC Complementary and Alternative Medicine, 13(1), 188. https://doi.org/10.1186/1472-6882-13-188

Nguyen, K. Van, Pongkitwitoon, B., Pathomwichaiwat, T., Viboonjun, U., & Prathanturarug, S. (2019). Effects of methyl jasmonate on the growth and triterpenoid production of diploid and tetraploid Centella asiatica (L.) Urb. hairy root cultures. Scientific Reports, 9(1), 18665. https://doi.org/10.1038/s41598-019-54460-z

Nurulita, N. A., Meiyanto, E., Sugiyanto, Matsuda, E., & Kawaichi, M. (2012). Gynura procumbens modulates the microtubules integrity and enhances distinct mechanism on doxorubicin and 5-flurouracil-induced breast cancer cell death. Oriental Pharmacy and Experimental Medicine, 12(3), 205–218. https://doi.org/10.1007/s13596-012-0063-5

Paek, K.-Y., Hahn, E.-J., & Son, S.-H. (2001). Application of bioreactors for large-scale micropropagation systems of plants. In Vitro Cellular & Developmental Biology - Plant, 37(2), 149–157. https://doi.org/10.1007/s11627-001-0027-9

Patil, R. A., Lenka, S. K., Normanly, J., Walker, E. L., & Roberts, S. C. (2014). Methyl jasmonate represses growth and affects cell cycle progression in cultured Taxus cells. Plant Cell Reports, 33(9), 1479–1492. https://doi.org/10.1007/s00299-014-1632-5

Puangpronpitag, D., Chaichanadee, S., Naowaratwattana, W., & Al, E. (2010). Gynura.. extract.pdf. In Asian Journal of Plant Sciences 9 (3): 146-151, 2010 ISSN 1682-3974 (Vol. 9, Issue 3).

Rahimi, S., Kim, Y.-J., & Yang, D.-C. (2015). Production of ginseng saponins: elicitation strategy and signal transductions. Applied Microbiology and Biotechnology, 99(17), 6987–6996. https://doi.org/10.1007/s00253-015-6806-8

Saiman, M. Z., Mustafa, N. R., Schulte, A. E., Verpoorte, R., & Choi, Y. H. (2012). Induction, characterization, and NMR-based metabolic profiling of adventitious root cultures from leaf explants of Gynura procumbens. Plant Cell, Tissue and Organ Culture (PCTOC), 109(3), 465–475. https://doi.org/10.1007/s11240-011-0111-8

See, K.S., Bhatt, A., Keng, C.L. (2011). Effect of sucrose and methyl jasmonate on biomass and anthocyanin production in cell suspension culture of Melastoma malabathricum (Melastomaceae). Rev Biol Trop, 59(2), 597-606. PMID: 21717852

Takanashi, K., Dan, K., Matsuoka, T., & Torii, K. (2019). The Cancer Cell Killing Effects of Gynura procumbens, Toleaf Are Associated with CD4+ T Lymphocyte Activation. Pharmaceutical Frontiers, :e190004, 1–13. https://doi.org/10.20900/pf20190004

Tan, H.-L., Chan, K.-G., Pusparajah, P., Lee, L.-H., & Goh, B.-H. (2016). Gynura procumbens: An Overview of the Biological Activities. Frontiers in Pharmacology, 7(52). https://doi.org/10.3389/fphar.2016.00052

Wang, Q., Wang, J., Chai, H., Li, J., Man, S., & Gao, W. (2015). Optimization of balloon-type bubble bioreactor angle and methyl jasmonate concentration to enhance metabolite production in adventitious roots of Pseudostellaria heterophylla. Research on Chemical Intermediates, 41(8), 5555–5563. https://doi.org/10.1007/s11164-014-1681-y

Wongwicha, W., Tanaka, H., Shoyama, Y., & Putalun,

W. (2011). Methyl Jasmonate Elicitation Enhances Glycyrrhizin Production in Glycyrrhiza inflata Hairy Roots Cultures. Zeitschrift Für Naturforschung C, 66(7–8), 423–428. https://doi.org/10.1515/znc-2011-7-815

Wu, S. Q., Lian, M. L., Gao, R., Park, S. Y., & Piao, X. C. (2011). Bioreactor application on adventitious root culture of Astragalus membranaceus. In Vitro Cellular & Developmental Biology - Plant, 47(6), 719–724. https://doi.org/10.1007/s11627-011-9376-1

Yi, T. G., Park, Y., Park, J.-E., & Park, N. Il. (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(7), 1–9. https://doi.org/10.1177/1934578X19861867

Yue, Y., Jiang, H., Du, J., Shi, L., Bin, Q., Yang, X., & Wang, L. (2019). Variations in physiological response and expression profiles of proline metabolism-related genes and heat shock transcription factor genes in petunia subjected to heat stress. Scientia Horticulturae, 258(108787), 1–10. https://doi.org/10.1016/j.scienta.2019.108811



DOI: https://doi.org/10.22146/mot.87736

Article Metrics

Abstract views : 1155 | views : 436

Refbacks

  • There are currently no refbacks.


Bookmark and Share


Copyright (c) 2024 Majalah Obat Tradisional

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

©Majalah Obat Tradisional (Traditional Medicine Journal)
 ISSN 2406-9086
Faculty of Pharmacy
Universitas Gadjah Mada