Skip to main content
SpringerLink
Log in

Differential Effects of Thidiazuron on Production of Anticancer Phenolic Compounds in Callus Cultures of Fagonia indica

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Fagonia indica, a very important anticancer plant, has been less explored for its in vitro potential. This is the first report on thidiazuron (TDZ)-mediated callogenesis and elicitation of commercially important phenolic compounds. Among the five different plant growth regulators tested, TDZ induced comparatively higher fresh biomass, 51.0 g/100 mL and 40.50 g/100 mL for stem and leaf explants, respectively, after 6 weeks of culture time. Maximum total phenolic content (202.8 μg gallic acid equivalent [GAE]/mL for stem-derived callus and 161.3 μg GAE/mL for leaf-derived callus) and total flavonoid content (191.03 μg quercetin equivalent [QE]/mL for stem-derived callus and 164.83 μg QE/mL for leaf-derived callus) were observed in the optimized callus cultures. The high-performance liquid chromatography (HPLC) data indicated higher amounts of commercially important anticancer secondary metabolites such as gallic acid (125.10 ± 5.01 μg/mL), myricetin (32.5 ± 2.05 μg/mL), caffeic acid (12.5 ± 0.52 μg/mL), catechin (9.4 ± 1.2 μg/mL), and apigenin (3.8 ± 0.45 μg/mL). Owing to the greater phenolic content, a better 2-2-diphenyl-1-picrylhydrazyl (DPPH) radical-scavenging activity (69.45 % for stem explant and 63.68 % for leaf explant) was observed in optimized calluses. The unusually higher biomass and the enhanced amount of phenolic compounds as a result of lower amounts of TDZ highlight the importance of this multipotent hormone as elicitor in callus cultures of F. indica.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Cancer 2015. Available from: http://www.who.int/mediacentre/factsheets/fs297/en/. Accessed 28 Jun 2015.

  2. Roleira, F. M., Tavares-da-Silva, E. J., Varela, C. L., Costa, S. C., Silva, T., Garrido, J., & Borges, F. (2015). Plant derived and dietary phenolic antioxidants: anticancer properties. Food Chemistry, 183, 235–258.

    Article  CAS  Google Scholar 

  3. Lam, M., Carmichael, A. R., & Griffiths, H. R. (2012). An aqueous extract of Fagonia cretica induces DNA damage, cell cycle arrest and apoptosis in breast cancer cells via FOXO3a and p53 expression. PloS One, 7, e40152.

    Article  CAS  Google Scholar 

  4. Waheed, A., Barker, J., Barton, S. J., Owen, C. P., Ahmed, S., & Carew, M. A. (2012). A novel steroidal saponin glycoside from Fagonia indica induces cell-selective apoptosis or necrosis in cancer cells. European Journal of Pharmaceutical Sciences, 47, 464–473.

    Article  CAS  Google Scholar 

  5. Saeed, M. A. (1969) Hamdard pharmacopoeia of Eastern medicine. pp. 41–43. Hamdard Academy, Karachi, Pakistan.

  6. Pareek, A., Godavarthi, A., Issarani, R., & Nagori, B. P. (2013). Antioxidant and hepatoprotective activity of Fagonia schweinfurthii (Hadidi) Hadidi extract in carbon tetrachloride induced hepatotoxicity in HepG2 cell line and rats. Journal of Ethnopharmacology, 150, 973–981.

    Article  Google Scholar 

  7. Saleem, S., Jafri, L., ul Haq, I., Chang, L. C., Calderwood, D., Green, B. D., & Mirza, B. (2014). Plants Fagonia cretica L. and Hedera nepalensis K. Koch contain natural compounds with potent dipeptidyl peptidase-4 (DPP-4) inhibitory activity. Journal of Ethnopharmacology, 156, 26–32.

    Article  CAS  Google Scholar 

  8. Alqasoumi, S. I., Yusufoglu, H. S., & Alam, A. (2011). Anti-inflammatory and wound healing activity of Fagonia schweinfurthii alcoholic extract herbal gel on albino rats. African Journal of Pharmacy and Pharmacology, 5, 1996–2001.

    Google Scholar 

  9. Rasool, B. K. A., Shehab, N. G., Khan, S. A., & Bayoumi, F. A. (2014). A new natural gel of Fagonia indica Burm f. extract for the treatment of burn on rats. Pakistan Journal of Pharmaceutical Sciences, 27, 73–81.

    Google Scholar 

  10. Bagban, I. M., Roy, S. P., Chaudhary, A., Das, S. K., Gohil, K. J., & Bhandari, K. K. (2012). Hepatoprotective activity of the methanolic extract of Fagonia indica Burm in carbon tetra chloride induced hepatotoxicity in albino rats. Asian Pacific Journal of Tropical Biomedicine, 2, S1457–S1460.

    Article  Google Scholar 

  11. Ansari, A. A., & Kenne, L. (1984). Hederagenin, ursolic acid, and pinatol from Fagonia indica. Journal of Natural Products, 47, 186–187.

    Article  Google Scholar 

  12. Shaker, K. H., Bernhardt, M., Elgamal, M. H. A., & Seifert, K. (2000). Sulfonated triterpenoid saponins from Fagonia indica. Zeitschrift Fur Naturforschung Section C-a Journal of Biosciences, 55, 520–523.

    CAS  Google Scholar 

  13. Khan, M. A., Abbasi, B., 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 Tissue Organic Culture, 120, 127–139.

    Article  CAS  Google Scholar 

  14. Matkowski, A. (2008). Plant in vitro culture for the production of antioxidants—a review. Biotechnology Advances, 26, 548–560.

    Article  CAS  Google Scholar 

  15. Davies, K. M., & Deroles, S. C. (2014). Prospects for the use of plant cell cultures in food biotechnology. Current Opinion in Biotechnology, 26, 133–140.

    Article  CAS  Google Scholar 

  16. Bahri-Sahloul, R., Ben Fredj, R., Boughalleb, N., Shriaa, J., Saguem, S., Hilbert, J.-L., Trotin, F., Ammar, S., Bouzid, S., & Harzallah-Skhiri, F. (2014). Phenolic composition and antioxidant and antimicrobial activities of extracts obtained from Crataegus azarolus L. var. aronia (Willd.) Batt. ovaries calli. Journal of Botany, 2014, 11.

    Article  Google Scholar 

  17. Slinkard, K., & Singleton, V. L. (1977). Total phenol analysis: automation and comparison with manual methods. American Journal of Enology and Viticulture, 28, 49–55.

    CAS  Google Scholar 

  18. Chang, C.-C., Yang, M.-H., Wen, H.-M. and Chern, J.-C. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis. 10.

  19. Shah, N. A., Khan, M. R., Naz, K., & Khan, M. A. (2014). Antioxidant potential, DNA protection, and HPLC-DAD analysis of neglected medicinal Jurinea dolomiaea roots. BioMed Research International, 2014, 726241.

    Google Scholar 

  20. Khan, M. A., Abbasi, B. H., Ahmed, N., & Ali, H. (2013). Effects of light regimes on in vitro seed germination and silymarin content in Silybum marianum. Industrial Crops and Products, 46, 105–110.

    Article  CAS  Google Scholar 

  21. Amarowicz, R., Pegg, R. B., Rahimi-Moghaddam, P., Barl, B., & Weil, J. A. (2004). Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chemistry, 84, 551–562.

    Article  CAS  Google Scholar 

  22. Murthy, B., Murch, S., & Saxena, P. K. (1998). Thidiazuron: a potent regulator of in vitro plant morphogenesis. In Vitro Cellular & Developmental Biology-Plant, 34, 267–275.

    Article  CAS  Google Scholar 

  23. Thomas, J. C., & Katterman, F. R. (1986). Cytokinin activity induced by thidiazuron. Plant Physiology, 81, 681–683.

    Article  CAS  Google Scholar 

  24. Eman, A. A., Gehan, H. A., Yassin, M., & Mohamed, S. (2010). Chemical composition and antibacterial activity studies on callus of Fagonia arabica L. Academia Arena, 2, 91–106.

    Google Scholar 

  25. Ebrahimi, M. A., & Payan, A. (2013). Induction of callus and somatic embryogenesis from cotyledon explants of Fagonia indica Burm. Journal of Medicinal Plants and By-Products, 2, 209–214.

    Google Scholar 

  26. Palmer, C. D., & Keller, W. (2011). Plant regeneration using immature zygotic embryos of Tribulus terrestris. Plant Cell, Tissue and Organ Culture, 105, 121–127.

    Article  Google Scholar 

  27. Mathur, S., & Shekhawat, G. S. (2013). Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiologiae Plantarum, 35, 931–939.

    Article  CAS  Google Scholar 

  28. Ali, M., & Abbasi, B. H. (2014). Thidiazuron-induced changes in biomass parameters, total phenolic content, and antioxidant activity in callus cultures of Artemisia absinthium L. Applied Biochemistry and Biotechnology, 172, 2363–2376.

  29. Nikam, T., Ebrahimi, M. A., & Patil, V. (2009). Embryogenic callus culture of Tribulus terrestris L. a potential source of harmaline, harmine and diosgenin. Plant Biotechnology Reports, 3, 243–250.

    Article  Google Scholar 

  30. Rice-Evans, C., Miller, N., & Paganga, G. (1997). Antioxidant properties of phenolic compounds. Trends in Plant Science, 2, 152–159.

    Article  Google Scholar 

  31. Pourebad, N., Motafakkerazad, R., Kosari-Nasab, M., Farsad Akhtar, N., & Movafeghi, A. (2015). The influence of TDZ concentrations on in vitro growth and production of secondary metabolites by the shoot and callus culture of Lallemantia iberica. Plant Cell, Tissue and Organ Culture, 122, 331–339.

    Article  CAS  Google Scholar 

  32. Bhargava, A., Clabaugh, I., To, J. P., Maxwell, B. B., Chiang, Y.-H., Schaller, G. E., Loraine, A., & Kieber, J. J. (2013). Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiology, 162, 272–294.

    Article  CAS  Google Scholar 

  33. Karam, N. S., Jawad, F. M., Arikat, N. A., & Shibl, R. A. (2003). Growth and rosmarinic acid accumulation in callus, cell suspension, and root cultures of wild Salvia fruticosa. Plant Cell, Tissue and Organ Culture, 73, 117–121.

    Article  CAS  Google Scholar 

  34. Shibli, R., Smith, M. A. L., & Kushad, M. (1997). Headspace ethylene accumulation effects on secondary metabolite production in Vaccinium pahalae cell culture. Plant Growth Regulation, 23, 201–205.

    Article  CAS  Google Scholar 

  35. Haslam, E., & Cai, Y. (1994). Plant polyphenols (vegetable tannins): gallic acid metabolism. Natural Product Reports, 11, 41–66.

    Article  CAS  Google Scholar 

  36. Mayr, C., Wagner, A., Neureiter, D., Pichler, M., Jakab, M., Illig, R., Berr, F., & Kiesslich, T. (2015). The green tea catechin epigallocatechin gallate induces cell cycle arrest and shows potential synergism with cisplatin in biliary tract cancer cells. BMC Complementary and Alternative Medicine, 15, 194.

    Article  Google Scholar 

  37. Nabavi, S., Habtemariam, S., Daglia, M. and Nabavi, S. (2015) Apigenin and breast cancers: from chemistry to medicine. Anti-Cancer Agents in Medicinal Chemistry.

  38. Rosendahl, A. H., Perks, C. M., Zeng, L., Markkula, A., Simonsson, M., Rose, C., Ingvar, C., Holly, J. M. P., & Jernström, H. (2015). Caffeine and caffeic acid inhibit growth and modify estrogen receptor and insulin-like growth factor I receptor levels in human breast cancer. Clinical Cancer Research, 21, 1877–1887.

    Article  CAS  Google Scholar 

  39. Subramanian, A. P., John, A. A., Vellayappan, M. V., Balaji, A., Jaganathan, S. K., Supriyanto, E., & Yusof, M. (2015). Gallic acid: prospects and molecular mechanisms of its anticancer activity. RSC Advances, 5, 35608–35621.

    Article  CAS  Google Scholar 

  40. Yi, J. L., Shi, S., Shen, Y. L., Wang, L., Chen, H. Y., Zhu, J., & Ding, Y. (2015). Myricetin and methyl eugenol combination enhances the anticancer activity, cell cycle arrest and apoptosis induction of cis-platin against HeLa cervical cancer cell lines. International Journal of Clinical and Experimental Pathology, 8, 1116–1127.

    CAS  Google Scholar 

  41. Chen, C.-H., Chan, H.-C., Chu, Y.-T., Ho, H.-Y., Chen, P.-Y., Lee, T.-H., & Lee, C.-K. (2009). Antioxidant activity of some plant extracts towards xanthine oxidase, lipoxygenase and tyrosinase. Molecules, 14, 2947.

    Article  CAS  Google Scholar 

  42. Abbasi, B., Khan, M., Mahmood, T., Ahmad, M., Chaudhary, M., & Khan, M. (2010). Shoot regeneration and free-radical scavenging activity in Silybum marianum L. Plant Cell, Tissue and Organ Culture, 101, 371–376.

    Article  CAS  Google Scholar 

  43. Camm, E. L., & Towers, G. N. (1973). Phenylalanine ammonia lyase. Phytochemistry, 12, 961–973.

    Article  CAS  Google Scholar 

  44. Schuster, B., & Retey, J. (1995). The mechanism of action of phenylalanine ammonia-lyase: the role of prosthetic dehydroalanine. Proceedings of the National Academy of Sciences, 92, 8433–8437.

    Article  CAS  Google Scholar 

  45. Nagai, N., Kitauchi, F., Okamoto, K., Kanda, T., Shimosaka, M., & Okazaki, M. (1994). A transient increase of phenylalanine ammonia-lyase transcript in kinetin-treated tobacco callus. Bioscience, Biotechnology, and Biochemistry, 58, 558–559.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Tariq Khan acknowledges the indigenous PhD fellowship program of the Higher Education Commission (HEC), Pakistan. Bilal Haider Abbasi acknowledges the financial support from the Pakistan Academy of Sciences (PAS), Pakistan.

Authors’ Contributions

TK did the research work and wrote the manuscript. BHA conceived the idea and supervised the work. MAK and BHA analyzed the data. BHA and ZKS critically reviewed the manuscript and added to its technical part.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Tariq Khan, Bilal Haider Abbasi & Zabta Khan Shinwari

  2. Biotechnology Program, Department of Environmental Sciences, COMSATS Institute of Information Technology (CIIT), Abbottabad, Pakistan

    Mubarak Ali Khan

  3. Pakistan Academy of Sciences, Islamabad, Pakistan

    Bilal Haider Abbasi & Zabta Khan Shinwari

Authors
  1. Tariq Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bilal Haider Abbasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mubarak Ali Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zabta Khan Shinwari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bilal Haider Abbasi.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, T., Abbasi, B.H., Khan, M.A. et al. Differential Effects of Thidiazuron on Production of Anticancer Phenolic Compounds in Callus Cultures of Fagonia indica . Appl Biochem Biotechnol 179, 46–58 (2016). https://doi.org/10.1007/s12010-016-1978-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-016-1978-y

Keywords

Search

Navigation