Abstract
In continuation of our work on Tagetes spp., the current study deals with the nematicidal activity of flavonoids, which are structurally related to two marker compounds, patuletin and patulitrin isolated from Tagetes patula flowers. The activity was determined against root-knot nematode, Meloidogyne incognita to establish structure activity relationship. In vitro examination of flavonoids belonging to flavone and flavonol classes revealed significant differences in nematicidal ability depending on their structural motif, concentration, and time of exposure. In case of flavonols the most efficient compounds were found to be fisetin, galangin, isorhamnetin, morin, and myricetin which exhibited 100% mortality of 2nd stage juveniles after 24 h of incubation. Whereas, among flavones which showed the same excellent activity parameters, were simple flavone, 6-hydroxy flavone, chrysin, 6-methoxy apigenin, apigenin-7-O-glucoside and 6-methoxy luteolin. These results revealed that flavonoids possess promising nematicidal activity and may have potential use in crop management as active agents.
Similar content being viewed by others
References
Adekunle, O. K., & Aderogba, M. A. (2008). Characterisation of an antinematicidal compoundfrom Leucaena leucocephala. Australasian Plant Disease Notes, 3(1), 168–170.
Ardakani, A. S. (2014). Compatibility of Heterorhabditis indica with neem seeds and kernel granules for suppressing Meloidogyne incognita infecting tomato. International Journal of Biosciences, 5(11), 114–121.
Bano, S., Faizi, S., Lubna, Fayyaz, S. & Iqbal, E. Y. (2019). Isolation of ceramides from Tagetes patula L. yellow flowers and nematicidal activity of the fractions and pure compounds against cyst nematode, Heterodera zeae. https://doi.org/10.1002/cbdv.201900092
Caboni, P., Saba, M., Tocco, G., Casu, L., Murgia, A., Maxia, A., Menkissoglu-Spiroudi, U., & Ntalli, N. (2013). Nematicidal activity of mint aqueous extracts against the root-knot nematode Meloidogyne incognita. Journal of Agricultural and Food Chemistry, 61(41), 9784–9788.
Chirumbolo, S. (2010). The role of quercetin, flavonols and flavones in modulating inflammatory cell function. Inflammation & Allergy Drug Targets, 9(4), 263–285.
Dayan, F. E., Cantrell, C. L., & Duke, S. O. (2009). Natural products in crop protection. Bioorganic & Medicinal Chemistry, 17(12), 4022–4034.
Dewick, P. M. (2009). The shikimate pathway: aromatic amino acids and phenylpropanoids. (In Medicinal natural products: a biosynthetic approach (3rd edition pp. 137–186). Chichester, UK: John Wiley and Sons, Ltd.)
Faizi, S., Siddiqi, H., Naz, A., Bano, S., & Lubna. (2010). Specific deuteration in patuletin and related flavonoids via keto-enoltautomerism: Solvent- and temperature-dependent 1H-NMR studies. Helvetica Chimica Acta, 93(3), 466–481.
Faizi, S., Fayyaz, S., Bano, S., Iqbal, E. Y., Lubna, Siddiqi, H., & Naz, A. (2011). Isolation of nematicidal compounds from Tagetes patula L. yellow flowers: Structure-activity relationship studies against cyst nematode Heterodera zeae infective stage larvae. Journal of Agricultural Food Chemistry, 59(17), 9080–9093.
Gattuso, G., Barreca, D., Gargiulli, C., Leuzzi, U., & Caristi, C. (2007). Flavonoid composition of Citrus juices. Molecules, 12(8), 1641–1673.
Ge, S., Gao, S., Yin, T., & Hu, M. (2015). Determination of pharmacokinetics of chrysin and its conjugates in wild-type FVB and Bcrp1 knockout mice using a validated LC-MS/MS method. Journal of Agricultural and Food Chemistry, 63(11), 2902–2910.
Gu, Y. Q., Mo, M. H., Zhou, J. P., Zou, C. S., & Zhang, K. Q. (2007). Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biology & Biochemistry, 39(10), 2567–2575.
Hussain, J., Ali, L., Khan, A. L., Najeeb-Ur-Rehman, Jabeen, F., Kim, J. S., & Al-Harrasi, A. (2014). Isolation and bioactivities of the flavonoids morin and morin-3-O-β-D-glucopyranoside from Acridocarpus orientalis-A wild Arabian medicinal plant. Molecules, 19(11), 17763–17772.
Jabeen, A.; Mesaik, M. A.; Simjee, S. U.; Lubna, Bano, S.; Faizi, S. (2016). Anti-TNF-α and anti-arthritic effect of patuletin: A rare flavonoid from Tagetes patula. International Immunopharmacology, 36, 232–240.
Jash, S. K., & Mondal, S. (2014). Bioactive flavonoid fisetin - A molecule of pharmacological interest. Journal of Organic Biomolecular Chemistry, 2(2), 89–128.
Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., Jones, M. G. K., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J. E., Wesemae, W. M. L., & Perry, R. N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14(9), 946–961.
Kale, V. M., & Namdeo, A. G. (2014). Antiarthritic effect of galangin isolated from rhizomes of Alpinia officinarum in complete freund’s adjuvant-induced arthritis in rats. International Journalof Pharmacy and Pharmaceutical Sciences, 6(4), 500–505.
Kashif, M., Bano, S., Naqvi, S., Faizi, S., Lubna, Mesaik, M. A., Azeemi, K. S. & Dar, A. (2015). Cytotoxic and antioxidant properties of phenolic compounds from Tagetes patula flowers. Pharmaceutical Biology, 53(5), 672–681.
Lago, J. H. G., Toledo-Arruda, A. C., Mernak, M., Barrosa, K. H., Martins, M. A., Tibério, I. F. L. C., & Prado, C. M. (2014). Structure-activity association of flavonoids in lung diseases. Molecule, 19(3), 3570–3595.
Li, N., Liu, J. H., Zhang, J., & Yu, B. Y. (2008). Comparative evaluation of cytotoxicity and antioxidative activity of 20 flavonoids. Journal of Agricultural and Food Chemistry, 56(10), 3876–3883.
Lilley, C. J., Kyndt, T. & Gheysen, G. (2011). Nematode resistant GM crops in industrialized and developing countries. In J. T. Jones, G. Gheysen & C. Fenoll (Eds.), Genomics and Molecular Genetics of Plant-Nematode Interactions (pp517–541). Heidelberg:Springer.
Lim, T. K. (2014). Tagetes patula. (in edible medicinal and non-medicinal plants, vol. 7 (pp 456-468), Netherland: Springer.)
Liu, A. L., Wang, H. D., Lee, S. M., Wang, Y. T., & Du, G. H. (2008). Structure activity relationship of flavonoids as influenza virus neuraminidase inhibitors and their in vitro anti-viral activities. Bioorganic& Medicinal Chemistry, 16(15), 7141–7147.
Lόpez-Lázaro, M. (2009). Distribution and biological activities of the flavonoid luteolin. Mini Reviews in Medicinal Chemistry, 9(1), 31–59.
Machado, A. R. T., Ferreira, S. R., Medeiros, F. D. S., Fujiwara, R. T., Filho, J. D. D. S., & Pimenta, L. P. S. (2015). Nematicidal activity of Annona crassiflora leaf extract on Caenorhabditis elegans. Parasites and Vectors, 8, 113–117.
Mahajan, R., Singh, P., & Bajaj, K. L. (1985). Nematicidal activity of some phenolic compounds against Meloidogyne incognita. Revue Nematology, 8(2), 161–164.
Mattivi, F., Guzzon, R., Vrhovsek, U., Stefanini, M., & Velasco, R. (2006). Metabolite profiling of grape: Flavonols and anthocyanins. Journal of Agricultural and Food Chemistry, 54(20), 7692–7702.
Munhoz, V. M., Baida, F. C., Lopes, G. C., Santiago, D. C., Souza, J. R. P., & Mello, J. C. P. (2017). Extracts and semi-purified fractions of Tagetes patula flowers in the control of root-knot nematodes. Semina: Ciencias Agrarias, Londrina, 38(6), 3529–3538.
Musarrat, A. R., Shahina, F., & Feroza, K. (2014). Systematic surveys of root-knot nematodes from rice and soybean fields of Pakistan. International Journal of Science Research, 3(10), 256–262.
Ntalli, N. G., & Caboni, P. (2012). Botanical nematicides: A review. Journal of Agricultural and Food Chemistry, 60(40), 9929–9940.
Patel, D. K., Patel, K., Gadewar, M., & Tahilyani, V. (2012). Pharmacological and bioanalytical aspects of galangin -a concise report. Asian Pacific Journal of Tropical Biomedicine, 2, S449–S455.
Pereira, O. R., Silva, A. M. S., Domingues, M. R. M., & Cardoso, S. M. (2012). Identification of phenolic constituents of Cytisus multiflorus. Food Chemistry, 131(2), 652–659.
Politi, F. A. S., Júnior, A. A. S., Fantatto, R. R., Pietro, R. C. L. R., Barioni, Júnior, W., Rabelo, M. D., Bizzo, H. R., Chagas, A. C. S., & Furlan, M. (2018). Chemical composition and in vitro anthelmintic activity of extracts of Tagetes patula against a multi drug-resistant isolate of Haemonchus contortus. Chemistry & Biodiversity, 15, e1700507. https://doi.org/10.1002/cbdv.201700507.
Ramesh, M., Narmadha, S., & Poopal, R. K. (2015). Toxicity of furadan (carbofuran 3% g) in Cyprinuscarpio: Haematological, biochemical and enzymological alterations and recovery response. Beni-Suef University Journal of Basic and Applied Sciences, 4(4), 314–326.
Saurabh, R., Gajendra, K. S., Badri, P. N., & Saroj, K. P. (2014). Extraction, isolation and chemical structure elucidation of isorhamnetin from leaves and stems of Agremone mexicana Linn of Bhopal, Madhya Pardesh, India. Indian Journal of Applied Research, 4(2), 10–13.
Shafaghat, A., & Salimi, F. (2008). Extraction and determining of chemical structure of flavonoids in Tanacetum parthenium (L.) Schultz. Bip from Iran. Journal of Science Islamic Azad University, 18(68), 39–42.
Tokuşoğlu, Ớ., Űnal, M. K., & Yildirim, Z. (2003). HPLC-UV and GC-MS characterization of the flavonol aglycone quercetin, kaempferol and myricetin in tomato pastes and other tomato based products. Acta Chromatographica, 13(3), 196–207.
Williams, C. (2013). Medicinal plants. (in Australia: An antipodean apothecary, Vol. 4 (pp 83-85). Australia: Rosenberg publishing).
Wuyts, N., Swennen, R., & De Waele, D. (2006). Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology, 8(1), 89–101.
Xu, S. L., Choi, R. C. Y., Zhu, K. Y., Leung, K. W., Guo, A. J. Y., Bi, D., Xu, H., Lau, D. T. W., Dong, T. T. X., & Tsim, K. W. K. (2012). Isorhamnetin, a flavonol aglycone from Ginkgo biloba L. induces neuronal differentiation of cultured PC12 cells: Potentiating the effect of nerve growth factor. Evidence-Based Complementary Alternative Medicine, 2012, 1–11. https://doi.org/10.1155/2012/278273.
Acknowledgements
Dr. Sadia Zik-ur-Rehman and Dr. Samina Bano were financially supported by Higher Education Commission Islamabad through Start-up Research Grant Program (SRGP) for the project entitled “Tagetes spp. A rich source of nematicidal agents” under Interim Placement of Fresh Ph.D’s (IPFP) program, and “Indigenous 5000 Fellowship Program (Batch-V)”, respectively.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
This research does not contain any conflicts of interest, nor research involving humans or animals.
Additional information
In memory of Prof. Dr. Salimuzzman Siddiqui FRS on his one hundred and twenty-third (123rd) birthday (October 19, 1897- April 14, 1994); he was the founding director of H.E.J Research Institute of Chemistry, University of Karachi.
Rights and permissions
About this article
Cite this article
Bano, S., Iqbal, E.Y., Lubna et al. Nematicidal activity of flavonoids with structure activity relationship (SAR) studies against root knot nematode Meloidogyne incognita. Eur J Plant Pathol 157, 299–309 (2020). https://doi.org/10.1007/s10658-020-01988-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-020-01988-w