Abstract
Fagonia indica Burm.f. (1768) is a medicinally important plant showing diverse pharmaceutical benefits. It is renowned for its ability to biosynthesize several anticancer and anti-inflammatory metabolites. For the eco-friendly and sustainable synthesis of phytochemicals and plant biomass, a biotechnological technique, “elicitation,” is a highly effective method in various in vitro cultures. The present study includes using various concentrations of Fusarium oxysporum Schlecht. as an elicitor in callus cultures of Fagonia indica. The main goal was to achieve enhancement in biomass production and secondary metabolism. The findings demonstrated that maximum biomass production (FW: 167.42 ± 3.99 g per 100 mL; DW: 12.53 ± 1.04 g per 100 mL) was observed at 50 mg L−1 of Fusarium oxysporum as compared to the control. Secondary metabolites showed immense production (phenolic content (9.68 ± 0.23 µg mg−1); flavonoid content (2.814808 ± 0.11 µg mg−1)) in callus cultures treated with 10 mg L−1 of Fusarium oxysporum as compared with control. Moreover, the cultures possessed the highest antioxidant capacity, as determined by 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS•+) radical cation based assay and α, α-diphenyl-β-picrylhydrazyl (DPPH) free radical scavenging assay, ((821.51 ± 3.20 µmol TEAC per mg DW of ABTS inhibition) (91% ± 1.45 of DPPH inhibition)) at 10 mg L−1 concentration of Fusarium oxysporum, and the maximum ferric ion reducing activity (219.29 ± 2.36 µmol TEAC per mg DW) was noticed at 1.0 mg L−1 concentration of F. oxysporum. Fagonia indica cultures also indicated the highest percent inhibition against cyclooxygenases (COX-1: 51.93% ± 1.74 and COX-2: 40.57% ± 1.99), lipoxygenase (15-LOX: 65.72% ± 1.44), and phospholipase A2 (sPLA2: 49.29% ± 1.75), when treated with different concentrations of F. oxysporum. HPLC analyses showed a significant accumulation of pharmacologically active components in the treated samples, with kaempferol (1245.56 mg g−1) and myricetin (1139.63 mg g−1) as the most accumulated compounds in the cultures with 10.0 mg L−1 concentration of Fusarium in contrast to the control. These findings revealed that in callus cultures of F. indica, F. oxysporum could boost biomass accumulation and secondary metabolite production.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Abbasi BH, Khan MA, Mahmood T, Ahmad M, Chaudhary MF, Khan MA (2010) Shoot regeneration and free-radical scavenging activity in Silybum marianum L. Plant Cell Tiss Org Cult 101:371–376
AbouZid S (2014) Yield improvement strategies for the production of secondary metabolites in plant tissue culture: silymarin from Silybum marianum tissue culture. Nat Prod Res 28:2102–2110. https://doi.org/10.1080/14786419.2014.927465
Ahmad N, Abbasi BH, Fazal H, Khan MA, Afridi MS (2014) Effect of reverse photoperiod on in vitro regeneration and piperine production in Piper nigrum L. Comptes Rendus Biolog 337:19–28
Ali AMA, El-Nour MEM, Yagi SM (2018) Total phenolic and flavonoid contents and antioxidant activity of ginger (Zingiber officinale Rosc.) rhizome, callus and callus treated with some elicitors. J Genet Eng Biotechnol 16:677–682
Ali K, Khan H (2021) Fagonia indica; areview on chemical constituents, traditional uses and pharmacological activities. Curr Pharm Des 27:2648–2660. https://doi.org/10.2174/1381612826666201210105941
Amarowicz R, Pegg RB, Rahimi-Moghaddam P, Barl B, Weil JA (2004) Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem 84:551–562
Azam F, Sheikh N, Ali G, Tayyeb A (2018) Fagonia indica repairs hepatic damage through expression regulation of toll-Like receptors in a liver injury model. J Immunol Res 2018:1–13. https://doi.org/10.1155/2018/7967135
Bading Taika B, Bouckandou M, Souza A, Bourobou Bourobou HP, MacKenzie LS, Lione L (2018) An overview of anti-diabetic plants used in Gabon: Pharmacology and toxicology. J ethnopharmacol 216:203–228. https://doi.org/10.1016/j.jep.2017.12.036
Baenas N, García-Viguera C, Moreno DA (2014) Elicitation: a tool for enriching the bioactive composition of foods. Molecules 19:13541–13563. https://doi.org/10.3390/molecules190913541
Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76. https://doi.org/10.1006/abio.1996.0292
Bhaskar R, Xavier LSE, Udayakumaran G, Kumar DS, Venkatesh R, Nagella P (2022) Biotic elicitors: a boon for the in-vitro production of plant secondary metabolites. Plant Cell Tiss Org Cult 149:7–24
Bourgeois C, Leclerc ÉA, Corbin C, Doussot J, Serrano V, Vanier JR, Seigneuret JM, Auguin D, Pichon C, Lainé É, Hano C (2016) Nettle (Urtica dioica L.) as a source of antioxidant and anti-aging phytochemicals for cosmetic applications. Comptes Rendus Chim 19:1090–1100. https://doi.org/10.1016/j.crci.2016.03.019
Buenger J, Ackermann H, Jentzsch A, Mehling A, Pfitzner I, Reiffen KA, Schroeder KR, Wollenweber U (2006) An interlaboratory comparison of methods used to assess antioxidant potentials 1. Int J Cosmet Sci 28:135–146
Chen SL, Yu H, Luo HM, Wu Q, Li CF, Steinmetz A (2016) Conservation and sustainable use of medicinal plants: problems, progress, and prospects. Chinese Med (united Kingdom) 11:1–10. https://doi.org/10.1186/s13020-016-0108-7
Daayf F, El Bellaj M, El Hassni M, J’aiti F, El Hadrami I (2003) Elicitation of soluble phenolics in date palm (Phoenix dactylifera) callus by Fusarium oxysporum f. sp. albedinis culture medium. Environ Exp Bot 49:41–47
Dimkić I, Janakiev T, Petrović M, Degrassi G, Fira D (2022) Plant-associated Bacillus and Pseudomonas antimicrobial activities in plant disease suppression via biological control mechanisms-a review. Physiol Mol Plant Pathol 117:101754
El-Aswad AF, Aly MI, Alsahaty SA, Basyony ABA (2023) Efficacy evaluation of some fumigants against Fusarium oxysporum and enhancement of tomato growth as elicitor-induced defense responses. Sci Rep 13:2479. https://doi.org/10.1038/s41598-023-29033-w
Fazal H, Abbasi BH, Ahmad N, Ali M (2016) Elicitation of medicinally important antioxidant secondary metabolites with silver and gold nanoparticles in callus cultures of prunella vulgaris L. Appl Biochem Biotechnol 180(6):1076–1092. https://doi.org/10.1007/s12010-016-2153-1
Fazili MA, Bashir I, Ahmad M, Yaqoob U, Geelani SN (2022) In vitro strategies for the enhancement of secondary metabolite production in plants: a review. Bull Natl Res Cent 46:1–12. https://doi.org/10.1186/s42269-022-00717-z
Graham JG, Quinn ML, Fabricant DS, Farnsworth NR (2000) Plants used against cancer - an extension of the work of Jonathan Hartwell. J Ethnopharmacol 73:347–377. https://doi.org/10.1016/S0378-8741(00)00341-X
Hada D, Sharma K (2016) Comparative analysis of different elicitors and binders and development of herbal formulation containing Cassia fistula L. fruit pulp against Alternaria solani. Int J Agric Sci 6:371–380
Hano C, Addi M, Bensaddek L, Crônier D, Baltora-Rosset S, Doussot J, Maury S, Mesnard F, Chabbert B, Hawkins S, Lainé E (2006) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223:975–989. https://doi.org/10.1007/s00425-005-0156-1
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:1–10. https://doi.org/10.3389/fpls.2019.00800
Kanwal I, Fatima N, Wazir A et al (2021) Fagonia Arabica Linn, a miraculous medicinal plant with diminutive scientific data but hefty potential. RADS J Pharm Pharmaceut Sci 9:185–189
Karwasara VS, Tomar P, Dixit VK (2011) Influence of fungal elicitation on glycyrrhizin production in transformed cell cultures of Abrus precatorius Linn. Pharmacogn Mag 7:307–313. https://doi.org/10.4103/0973-1296.90411
Khan MA, Abbasi BH, Ali H, Ali M, Adil M, Hussain I (2015) Temporal variations in metabolite profiles at different growth phases during somatic embryogenesis of Silybum marianum L. Plant Cell Tiss Org Cult 120:127–139
Khan T, Abbasi B, Khan M, Shinwari Z (2016) Differential effects of thidiazuron on production of anticancer phenolic compounds in callus cultures of Fagonia indica. Appl Biochem Biotechnol 179:46–58. https://doi.org/10.1007/s12010-016-1978-y
Khan T, Abbasi BH, Khan MA, Azeem M (2017) Production of biomass and useful compounds through elicitation in adventitious root cultures of Fagonia indica. Ind Crops Prod 108:451–457. https://doi.org/10.1016/j.indcrop.2017.07.019
Khan T, Khan T, Hano C, Abbasi BH (2019) Effects of chitosan and salicylic acid on the production of pharmacologically attractive secondary metabolites in callus cultures of Fagonia indica. Ind Crops Prod 129:525–535. https://doi.org/10.1016/j.indcrop.2018.12.048
Kolewe ME, Gaurav V, Roberts SC (2008) Pharmaceutically active natural product synthesis and supply via plant cell culture technology. Mol Pharm 5:243–256. https://doi.org/10.1021/mp7001494
Laroche C, Gervais P (2003) Achievement of rapid osmotic dehydration at specific temperatures could maintain high Saccharomyces cerevisiae viability. Appl Microbiol Biotechnol 60:743–747. https://doi.org/10.1007/s00253-002-1167-5
Latif A, Abbas N, Waheed I, Qaisar MN (2019) Alpha-glucosidase inhibitory and antioxidant activities of various extracts of aerial parts of Fagonia indica Burm. F. Trop J Pharma Res 18:791–797
Michiels JA, Kevers C, Pincemail J, Defraigne JO, Dommes J (2012) Extraction conditions can greatly influence antioxidant capacity assays in plant food matrices. Food Chem 130:986–993
Miranda CL, Kumbi Y, Wu W et al (2022) Phytochemical characterization and bioactivity toward breast cancer cells of unhydrolyzed and acid-hydrolyzed extracts of Fagonia indica. Nat Prod Comm 17:1–12
Morel G, Wetmore RH (1951) Tissue culture of monocotyledons. Am J Bot 38:138–140
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Oguntibeju OO (2018) Medicinal plants with anti-inflammatory activities from selected countries and regions of Africa. J Inflamm Res 11:307–317. https://doi.org/10.2147/JIR.S167789
Otho AA, Memon RA, Abro SA, Memon AA (2021) Elemental analysis of medicinal herb Fagonia indica Burm. f. and its rhizospheric soil from six geographical locations of south-eastern sindh province, Pakistan, during spring and summer seasons. Biol Trace Elem Res 200:2439–2454. https://doi.org/10.1007/s12011-021-02873-1
Petruk G, Del GR, Rigano MM, Monti DM (2018) Antioxidants from plants protect against skin photoaging. Oxidat Med Cell Longevity 2018:1454936. https://doi.org/10.1155/2018/1454936
Plaza A, Rodríguez L, Concha-Meyer AA, Cabezas R, Zurob E, Merlet G, Palomo I, Fuentes E (2023) Effects of extraction methods on phenolic content, antioxidant and antiplatelet activities of tomato pomace extracts. Plants 12:1188–1208
Pleadin J, Frece J, Markov K (2019) Mycotoxins in food and feed. Adv Food Nutr Res 89:297–345
Puri D, Bhandari A (2015) Fagonia: a potential medicinal desert plant. J Nepal Pharm Assoc 27:28–33. https://doi.org/10.3126/jnpa.v27i1.12147
Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Golenioswki CRM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182–206. https://doi.org/10.3390/molecules21020182
Ribeiro D, Freitas M, Lima JLFC, Fernandes E (2015) Proinflammatory pathways: the modulation by flavonoids. Med Res Rev 35:877–936
Sák M, Dokupilová I, Kaňuková Š, Mrkvová M, Mihálik D, Hauptvogel P, Kraic J (2021) Biotic and abiotic elicitors of stilbenes production in Vitis vinifera L. Cell Culture. Plants 10:1–14. https://doi.org/10.3390/plants10030490
Semwal DK, Semwal RB, Combrinck S, Viljoen A (2016) Myricetin: a dietary molecule with diverse biological activities. Nutrients 8:90–121. https://doi.org/10.3390/nu8020090
Shehab NG, Abu-Gharbieh E, Bayoumi FA (2015) Impact of phenolic composition on hepatoprotective and antioxidant effects of four desert medicinal plants. BMC Complement Altern Med 15:1–12
Shrestha PM, Dhillion SS (2006) Diversity and traditional knowledge concerning wild food species in a locally managed forest in Nepal. Agrofor Syst 66:55–63
Tagliazucchi D, Verzelloni E, Bertolini D, Conte A (2010) In vitro bio-accessibility and antioxidant activity of grape polyphenols. Food Chem 120:599–606. https://doi.org/10.1016/j.foodchem.2009.10.030
Ullah A, Munir S, Badshah SL, Khan N, Ghani L, Poulson BG, Emwas AH, Jaremko M (2020) Important flavonoids and their role as a therapeutic agent. Molecules 25:5243. https://doi.org/10.3390/molecules25225243
Waheed A, Barker J, Barton SJ, Owen CP, Ahmed S, Carew MA (2012) A novel steroidal saponin glycoside from Fagonia indica induces cell-selective apoptosis or necrosis in cancer cells. Eur J Pharm Sci 47:464–473. https://doi.org/10.1016/j.ejps.2012.07.004
Wang Y, Li S, Han D, Meng K, Wang M, Zhao C (2015) Simultaneous determination of rutin, luteolin, quercetin, and betulinic acid in the extract of Disporopsis pernyi (Hua) Diels by UPLC. J Anal Methods Chem 2015:525–535. https://doi.org/10.1155/2015/130873
Warhade MI, Badere RS (2018) Fusarium oxysporum cell elicitor enhances betalain content in the cell suspension culture of Celosia cristata. Physiol Mol Biol Plants 24:285–293. https://doi.org/10.1007/s12298-018-0511-x
Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant Microbe Interact 17:1385–1393. https://doi.org/10.1094/MPMI.2004.17.12.1385
Yin S, Gao Z, Wang C, Huang L, Kang Z, Zhang H (2016) Nitric oxide and reactive oxygen species coordinately regulate the germination of Puccinia striiformis f. sp. tritici urediniospores. Front Microbiol 7:178
Zaletok S, Gulua L, Wicker L, Shlyakhovenko V, Gogol S, Orlovsky O, Karnaushenko O, Verbinenko A, Milinevska V, Samoylenko O, Todor I (2015) Green tea, red wine and lemon extracts reduce experimental tumor growth and cancer drug toxicity. Exp Oncol 37:262–271
Zhong L, Niu B, Tang L, Chen F, Zhao G, Zhao J (2016) Effects of polysaccharide elicitors from endophytic Fusarium oxysporum Fat9 on the growth, flavonoid accumulation and antioxidant property of Fagopyrum tataricum sprout cultures. Molecules 21(12):1590–1603. https://doi.org/10.3390/molecules21121590
Acknowledgements
BHA gratefully acknowledges the research fellowship of Le Studium, Institute of Advanced Studies, Orléans France.
Author information
Authors and Affiliations
Contributions
Taimoor Khan performed the experiments. Razia Khurshid and Gouhar Zaman assisted Taimoor Khan in performing the experiments. HPLC analysis and interpretations were done by Christophe Hano. TPC, TFC, and Antioxidant activites were performed by Muhammad Uzair Javed. Tariq Khan performed Anti-inflammatory activities and critically reviewed the manuscript. The manuscript was drafted by Tehreem Mahmood and Bushra Khan and all authors commented on previous versions of the manuscript. Bilal Haider Abbasi conceived the idea, facilitated and supervised the research.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval
Not applicable
Consent to participate
Not applicable
Consent to publish
Not applicable
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Khan, T., Javed, M.U., Mahmood, T. et al. Enhancement in the production of phenolic compounds from Fagonia indica callus cultures via Fusarium oxysporum triggered elicitation. In Vitro Cell.Dev.Biol.-Plant 60, 16–27 (2024). https://doi.org/10.1007/s11627-023-10358-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-023-10358-0