Skip to main content
SpringerLink
Log in

Study of sodium 3-hydroxycoumarin as inhibitors in vitro, in vivo and in silico of Moniliophthora perniciosa fungus

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

The inhibition of the fungus Moniliophthora perniciosa, which is the causal agent of witches’ broom disease in Theobroma cacao L., is the main focus of the present study. The use of phytoalexins has provided disease control that is as efficient as control with the use of fungicides, with the advantage of not harming humans and the environment. In this sense, the objective was to evaluate the action of 3-hydroxycoumarin compared with the standard defence activator acibenzolar-S-methyl (Bion® 500 WG) and systemic fungicide tebuconazole (Folicur® 200 CE), and study the possible mechanisms of action. Initially, basidiospore germination inhibition assays (in vitro) were performed using four different concentrations of 3-hydroxycoumarin. The result was 100% inhibition at the concentration of 1000 ppm. Thereafter, this substance was used in four different treatments (in vivo) of cacao seedlings of the SIC-23 genotype, with regard to the order of application. The data analysis showed greater inhibition when 3-hydroxycoumarin was applied after inoculation (TAI test), and suggested a curative effect on Theobroma cacao seedlings. In silico, it was used the enzyme chitin synthase because this action as key enzyme in chitin biosynthetic pathway. The in silico tests show that 3-hydroxycoumarin inhibited the production of chitin synthase by the fungus. Therefore, the present study identifies a potential inhibitor of M. perniciosa and suggests the best application methodology.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aime, M. C., & Phillips-Mora, W. (2005). The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia, 97, 1012–1022.

    CAS  PubMed  Google Scholar 

  • Al-Amiery, A. A., Al-Bayati, R. I. H., Saour, K. Y., & Radi, M. F. (2011). Cytotoxicity, antioxidant, and antimicrobial activities of novel 2-quinolone derivatives derived from coumarin. Research on Chemical Intermediates, 38, 559–569.

    Article  CAS  Google Scholar 

  • Al-Amiery, A. A., Kadhum, A. A. H., & Mohamad, A. B. (2012). Antifungal activities of new coumarins. Molecules, 17, 5713–5723.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ampasala, D. R., Zheng, S., Zhang, D., Ladd, T., Doucet, D., Krell, P. J., Retnakaran, A., & Feng, Q. (2011). An epidermis-specific chitin synthase cdna in Choristoneura fumiferana: Cloning, characterization, developmental and hormonal-regulated expression. Archives of Insect Biochemistry and Physiology, 76(2), 83–96.

    Article  CAS  PubMed  Google Scholar 

  • Atmaka, M., Bilgin, H. M., Obay, B. D., Diken, H., Kelle, M., & Kale, E. (2011). The hepatoprotective effect of coumarin and coumarin derivatives on carbon tetrachloride-induced hepatic injury by anti-oxidative activities in rats. Journal of Physiology and Biochemistry, 67, 569–576.

    Article  CAS  Google Scholar 

  • Bansal, Y., Sethi, P., & Bansal, G. (2013). Coumarin: A potential nucleus for anti-inflammatory molecules. Medicinal Chemistry Research, 22, 3049–3060.

    Article  CAS  Google Scholar 

  • Behr, J. B. (2003). Chitin synthase as an antifungal target: Recent advances. Current Medicinal Chemistry, 2, 173–189.

    CAS  Google Scholar 

  • Carpinella, M. C., Ferrayoli, C. G., & Palacios, S. M. (2005). Antifungal synergistic effect of scopoletin, a hydroxycoumarin isolated from Melia azedarach L. fruits. Agricultural and Food Chemistry, 53, 2922–2927.

    Article  CAS  Google Scholar 

  • Case, D. A., Darden, T. A., Cheatham III, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goets, A. W., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M. J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., Kollman, P. A. (2012), AMBER 12, University of California, San Francisco.

  • Dhanavade, M. J., Jalkute, C. B., Ghosh, J. S., & Sonawane, K. D. (2011). Study antimicrobial activity of lemon (Citrus Lemon L.) peel extract. British Journal of Pharmacology and Toxicology, 2, 119–122.

    Google Scholar 

  • Duo-Chuan, L. (2006). Review of fungal chitinases. Mycopathologia, 161, 345–360.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, S. Z., Carneiro, H. C., Lara, H. A., Alves, R. B., Resende, J. M., Oliveira, H. M., & Freitas, R. P. (2015). Synthesis of a new peptide–coumarin conjugate: A potential agent against Cryptococcosis. ACS Medicinal Chemistry Letters, 6, 271–275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frias, G. A., Purdy, L. H., & Schmidt, R. A. (1995). An inoculation method for evaluate resistance of cocoa to Crinipellis perniciosa. Plant Disease, 79, 787–791.

    Article  Google Scholar 

  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Petersson, G. A., Nakatsuji, H., Li, X., Caricato, M., Marenich, A., Bloino, J., Janesko, B. G., Gomperts, R., Mennucci, B., Hratchian, H. P., Ortiz, J. V., Izmaylov, A. F., Sonnenberg, J. L., Williams-Young, D., Ding, F., Lipparini, F., Egidi, F., Goings, J., Peng, B., Petrone, A., Henderson, T., Ranasinghe, D., Zakrzewski, V. G., Gao, J., Rega, N., Zheng, G., Liang, W., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Throssell, K., Montgomery, Jr., J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Keith, T., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Millam, J. M., Klene, M., Adamo, C., Cammi, R., Ochterski, J. W., Martin, R. L., Morokuma, K., Farkas, O., Foresman, J. B., and Fox, D. J., Gaussian, Inc., Wallingford CT, 2016.

  • Godoy, M. F. P., Victor, S. R., Bellini, A. M., Guerreiro, G., Rocha, W. C., Bueno, O. C., Hebling, M. J. A., Bacci Jr., M., Silva, M. F. G. F., Vieira, P. C., Fernandes, J. B., & Pagnocca, F. C. (2005). Inhibition of the symbiotic fungus of leaf-cutting ants by coumarins. Journal of the Brazilian Chemical Society, 16, 669–672.

    Article  CAS  Google Scholar 

  • Gramacho, K. P., Luz, E. D. M. N., Silva, F. S., Lopes, U. V., Pires, J. L., & Pereira, L. (2016). Pathogenic variability of Moniliophthora perniciosa in three agroecological zones of the cacao region of Bahia, Brazil. Crop Breeding and Applied Biotechnology, 16, 7–13.

    Article  CAS  Google Scholar 

  • Johann, S., Mendes, B. G., Missau, F. C., Resende, M. A., & Pizzolatti, M. G. (2011). Antifungal activity of five species of Polygala. Brazilian Journal of Microbiology, 42, 1065–1075.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karatas, M. O., Olgundeniz, B., Günal, S., Özdemir, I., Alici, B., & Çetinkaya, E. (2016). Synthesis, characterisation and antimicrobial activities of novel silver(I) complexes with coumarin substituted N-heterocyclic carbene ligands. Bioorganic & Medicinal Chemistry, 24, 643–650.

    Article  CAS  Google Scholar 

  • Kasumbwe, K., Venugopala, K. N., Mohanlall, V., & Odhav, B. (2014). Antimicrobial and antioxidant activities of substituted halogenated coumarins. Journal of Medicinal Plant Research, 5, 274–281.

    Article  CAS  Google Scholar 

  • Kerrigan, J. E. (2009). Amber 9.0 Drug/DNA complex. Piscataway, New Jersey, p. 17.

  • Krumrine, J., Raubacher, F., Brooijmans, N., & Kuntz, I. (2003). Principles and methods of docking and ligand design. In P. E. Bourne & W. Helge (Eds.), Structural Bioinformatics (pp. 443–476). New Jersey: John Wiley & Sons.

  • Lagorce, A., Le Berre-Anton, V., Aguilar-Uscanga, B., Martin-Yken, H., Dagkessamanskaia, A., & François, J. (2002). Activation of the chitin synthesis pathway in response to cell-wall defects in Saccharomyces cerevisiae. European Journal of Biochemistry, 269, 1697–1707.

    Article  CAS  PubMed  Google Scholar 

  • Leal, L. K. A. M., Ferreira, A. A. G., Bezerra, G. A., Matos, F. J. A., & Viana, G. S. B. (2000). Anti-nociceptive, anti-inflammatory and bronchodilator activities of Brazilian medicinal plants containing coumarin: A comparative study. Journal of Ethnopharmacology, 70, 151–150.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., Li, F., Li, D., Ma, E., Zhang, W., Zhu, K. Y., & Zhang, J. (2013). Molecular and functional analysis of UDP-N-Acetylglucosamine pyrophosphorylases from the migratory locust, locusta migratoria. PLoS One, 8(8), e71970. Published online 2013 Aug 19. https://doi.org/10.1371/journal.pone.0071970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meinhardt, L. W., Rincones, J., Bailey, B. A., Aime, M. C., Griffith, G. W., & Zhang, D. (2008). Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: what’s new from this old foe? Molecular Plant Pathology, 9, 577–588.

    Article  PubMed  Google Scholar 

  • Miyano, D. M., Lima, T., Simões, F. R., La-Scalea, M. A., Oliveira, h. P. M., & Codognoto, L. (2014). Electrochemical study of simple coumarin and its determination in aqueous infusion of Mikania glomerata. Journal of Brazilian Chemical Society, 25, 602–609.

    CAS  Google Scholar 

  • Mouri, T., Yano, T., Kochi, S., Ando, T., & Hori, M. (2005). Synthesis and antifungal activity of new 3,4,7-tri-substituted coumarins. Journal of Pesticide Science, 30, 209–213.

    Article  CAS  Google Scholar 

  • Rehman, S. U., Chohan, Z. H., Gulnaz, F., & Supuran, C. T. (2005). In-vitro antibacterial, antifungal and cytotoxic activities of some coumarins and their metal complexes. Journal of Enzyme Inhibition and Medicinal Chemistry, 20, 333–340.

    Article  CAS  PubMed  Google Scholar 

  • Rino, J. P., & Studart, N. (2001). Um potencial de interação para o estudo de materiais e simulações por dinâmica molecular. Química Nova, 24, 838–845.

    Article  CAS  Google Scholar 

  • Roncero, C. (2002). The genetic complexity of chitin synthesis in fungi. Current Genetics, 41, 367–378.

    Article  CAS  PubMed  Google Scholar 

  • Scarpari, l. M., Meinhardt, l. W., Mazzafera, P., Pomella, A. W. V., Schiavinato, M. A., Cascardo, J. C. M., & Pereira, G. A. G. (2005). Biochemical changes during the development of witches’ broom: The most important disease of cocoa in Brazil caused by Crinipellis perniciosa. Journal of Experimental Botany, 56, 856–877.

    Article  CAS  Google Scholar 

  • Shi, Y., Zhou, C. H., Zhou, X. D., Geng, R. X., & Ji, Q. G. (2011). Synthesis and antimicrobial evaluation of coumarin-based benzotriazoles and their synergistic effects with chloromycin and fluconazole. Acta Pharmaceutica Sinica, 46, 798–810.

    CAS  PubMed  Google Scholar 

  • Singh, L. K., Priyanka, Singh, V., & Katiyar, D. (2015). Design, synthesis and biological evaluation of some new coumarin derivatives as potential antimicrobial agents. Medicinal Chemistry, 11, 128–134.

    Article  CAS  PubMed  Google Scholar 

  • Souza, C. S., Oliveira, B. M., Costa, G. G. L., Schriefer, A., Schnadelbach, A. S., Uetanabaro, A. P. T., Pirovani, C. P., Pereira, G. A., Taranto, A. G., Cascardo, J. C. M., & Goes-Neto, A. (2009). Identification and characterization of a class III chitin synthase gene of Monilliophthora perniciosa, the fungus that causes witches' broom disease of cacao. Journal of Microbiology, 47, 431–440.

    Article  CAS  Google Scholar 

  • Stein, A. C., Alvarez, S., Avancini, C., Zacchino, S., & von Poser, G. (2006). Antifungal activity of some coumarins obtained from species of Pterocaulon (Asteraceae). Journal of Ethnopharmacology, 107, 95–98.

    Article  CAS  PubMed  Google Scholar 

  • Stewart, J. J. P. (2007). Optimization of parameters for semi-empirical methods V: Modification of NDDO approximations and application to 70 elements. Journal of Molecular Modeling, 13, 1173–1213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulimov, A. V., Kutov, D. C., Katkova, E. V., Ilin, I. S., & Sulimov, V. B. (2017). New generation of docking programs: Supercomputer validation of force fields and quantum-chemical methods for docking. Journal of Molecular Graphics and Modelling, 78, 139–147.

    Article  CAS  PubMed  Google Scholar 

  • Trott, O., & Olson, A. J. (2010). AutoDockVina: Improvising the speed and accuracy of docking with a new scoring function, efficient optimisation and multithreading. Journal of Computational Chemistry, 31, 455–461.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venugopala, K. N., Rashmi, V., & Odhav, B. (2013). Review on natural coumarin lead compounds for their pharmacological activity. BioMed Research International. https://doi.org/10.1155/2013/963248.

  • Yadav, I. S., Nandekar, P. P., Shrivastava, S., Sangamwar, A., Chaudhury, A., & Agarwal, S. M. (2014). Ensemble docking and molecular dynamics identify knoevenagel curcumin derivatives with potent anti-EGFR activity. Gene, 539(1), 82–90.

    Article  CAS  PubMed  Google Scholar 

  • Yeager, A. R., & Finney, N. S. (2004). The first direct evaluation of the two-active site mechanism for chitin synthase. The Journal of Organic Chemistry, 69(3), 613–618.

    Article  CAS  PubMed  Google Scholar 

  • Young, D. C. (2009). Computational drug design: a guide for computational and medicinal chemists. John Wiley & Sons.

Download references

Author information

Authors and Affiliations

  1. Departamento de Saúde, Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, 44031-460, Brazil

    Priscila de Andrade Gonçalves, Manoelito Coelho dos Santos Junior & Sandra Aparecida de Assis

  2. Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, 44031-460, Brazil

    Catiane do Sacramento Sousa & Aristóteles Góes-Neto

  3. CEPLAC, Centro de Pesquisas do Cacau (CEPEC), Rod. Ilhéus-Itabuna, km 22, Itabuna, Bahia, 45.600-000, Brazil

    Edna Dora Martins Newman Luz, Virgínia Oliveira Damaceno & Ana Rosa Rocha Niella

  4. Departamento de Saúde, Universidade Federal da Paraíba, João Pessoa, Paraíba, 55037-685, Brazil

    José Maria Barbosa Filho

Authors
  1. Priscila de Andrade Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manoelito Coelho dos Santos Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catiane do Sacramento Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aristóteles Góes-Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edna Dora Martins Newman Luz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Virgínia Oliveira Damaceno
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ana Rosa Rocha Niella
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. José Maria Barbosa Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sandra Aparecida de Assis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandra Aparecida de Assis.

Ethics declarations

Conflict of interest

The authors state that there are no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Andrade Gonçalves, P., dos Santos Junior, M.C., do Sacramento Sousa, C. et al. Study of sodium 3-hydroxycoumarin as inhibitors in vitro, in vivo and in silico of Moniliophthora perniciosa fungus. Eur J Plant Pathol 153, 15–27 (2019). https://doi.org/10.1007/s10658-018-1536-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-018-1536-2

Keywords

Search

Navigation