Abstract
The effectiveness of some plant extracts to protect crops against pests enhancing the natural defensive responses of the plant has been previously reported. Plant extract of Mimosa tenuiflora and Quercus robur has promising potential to reduce the incidence of a wide range of phytopathogenic fungi due to its antimicrobial compounds. In this study, we aimed to elucidate the effectiveness and the mode of action of this mix extract in Lactuca sativa against Sclerotinia sclerotiorum. To achieve this objective, 4 weeks old lettuce plants of cv. Romana were treated with 2 cc l−1 of the plant extract either by soil drench or foliar applications 72 h before the inoculation. The treatments were able to significantly reduce the progression of the pathogen, decreasing the diameter of the infection by 32% and 17% in foliar and soil drench application, respectively. Moreover, the results showed significantly higher levels of hydrogen peroxide (H2O2) as well as callose deposition in plants treated and inoculated, compared with non-treated plants. However, no direct effect on the fungus growth was observed in vitro suggesting that foliar and soil drench treatments with M. tenuiflora and Q. robur extract significantly reduce the infection of S. sclerotiorum in leaves of lettuce, through the strengthening of the wall mediated by the deposition of callose and the release of H2O2. The fact that the treatment enhances different processes involved in plant innate defense may indicate that this treatment is acting as a resistant inducer, and could be effective against different microorganisms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbasi, P. A., Cuppels, D. A., & Lazarovits, G. (2003). Effect of foliar applications of neem oil and fish emulsion on bacterial spot and yield of tomatoes and peppers. Canadian Journal of Plant Pathology, 25(1), 41–48. https://doi.org/10.1080/07060660309507048.
Amadioha, A. C. (2000). Controlling rice blast in vitro and in vivo with extracts of Azadirachta indica. Crop Protection, 19(5), 287–290. https://doi.org/10.1016/S0261-2194(99)00080-0.
Andrenšek, S., Simonovska, B., Vovk, I., Fyhrquist, P., Vuorela, H., & Vuorela, P. (2004). Antimicrobial and antioxidative enrichment of oak (Quercus robur) bark by rotation planar extraction using ExtraChrom®. International Journal of Food Microbiology, 92(2), 181–187. https://doi.org/10.1016/J.IJFOODMICRO.2003.09.009.
Azevedo, L., Chagas-Paula, D. A., Kim, H., Roque, A. C. M., Dias, K. S. T., Machado, J. C., et al. (2016). White mold (Sclerotinia sclerotiorum), friend or foe: Cytotoxic and mutagenic activities in vitro and in vivo. Food Research International, 80, 27–35. https://doi.org/10.1016/J.FOODRES.2015.11.029.
Burketova, L., Trda, L., Ott, P. G., & Valentova, O. (2015). Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnology Advances, 33(6), 994–1004. https://doi.org/10.1016/J.BIOTECHADV.2015.01.004.
Chen, Y., Gao, X., Chen, Y., Qin, H., Huang, L., & Han, Q. (2014). Inhibitory efficacy of endophytic Bacillus subtilis EDR4 against Sclerotinia sclerotiorum on rapeseed. Biological Control, 78, 67–76. https://doi.org/10.1016/J.BIOCONTROL.2014.07.012.
Clarkson, J. P., Fawcett, L., Anthony, S. G., & Young, C. (2014). A model for Sclerotinia sclerotiorum infection and disease development in lettuce, based on the effects of temperature, relative humidity and Ascospore density. PLoS One, 9(4), e94049. https://doi.org/10.1371/journal.pone.0094049.
da Cruz Cabral, L., Fernández Pinto, V., & Patriarca, A. (2013). Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. International Journal of Food Microbiology, 166(1), 1–14. https://doi.org/10.1016/j.ijfoodmicro.2013.05.026.
Davidson, A. L., Blahut-Beatty, L., Itaya, A., Zhang, Y., Zheng, S., & Simmonds, D. (2016). Histopathology of Sclerotinia sclerotiorum infection and oxalic acid function in susceptible and resistant soybean. Plant Pathology, 65(6), 878–887. https://doi.org/10.1111/ppa.12514.
de Souza Araújo, E., Pimenta, A. S., Feijó, F. M. C., Castro, R. V. O., Fasciotti, M., Monteiro, T. V. C., & de Lima, K. M. G. (2018). Antibacterial and antifungal activities of pyroligneous acid from wood of Eucalyptus urograndis and Mimosa tenuiflora. Journal of Applied Microbiology, 124(1), 85–96. https://doi.org/10.1111/jam.13626.
Ellinger, D., Naumann, M., Falter, C., Zwikowics, C., Jamrow, T., Manisseri, C., et al. (2013). Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiology, 161(3), 1433–1444. https://doi.org/10.1104/pp.112.211011.
Fernández-Crespo, E., Scalschi, L., Llorens, E., García-Agustín, P., Camañes, G., Fernández-Crespo, E., et al. (2015). NH4+ protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. Journal of Experimental Botany, 66(21), 6777–6790. https://doi.org/10.1093/jxb/erv382.
Ferreira, M. R. A., Santiago, R. R., Langassner, S. M. Z., Palazzo De Mello, J. C., Svidzinski, T. I. E., Soares, L. A. L. (2013). Antifungal activity of medicinal plants from Northeastern Brazil, 7(40), 3008–3013. doi:https://doi.org/10.5897/JMPR2013.5035
Gahukar, R. T. (2012). Evaluation of plant-derived products against pests and diseases of medicinal plants: A review. Crop Protection, 42, 202–209. https://doi.org/10.1016/J.CROPRO.2012.07.026.
González-Hernández, A. I., Llorens, E., Agustí-Brisach, C., Vicedo, B., Yuste, T., Cerveró, A., et al. (2018). Elucidating the mechanism of action of copper heptagluconate on the plant immune system against Pseudomonas syringae in tomato ( Solanum lycopersicum L). Pest Management Science. https://doi.org/10.1002/ps.5050.
Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J.-M., & Mauch-Mani, B. (2005). β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of Callose formation and Jasmonic acid signaling. Molecular Plant-Microbe Interactions, 18(8), 819–829. https://doi.org/10.1094/MPMI-18-0819.
Heffer. (2007). White Mold. The Plant Health Instructor. https://doi.org/10.1094/PHI-I-2007-0809-01.
Ji, H., Kyndt, T., He, W., Vanholme, B., & Gheysen, G. (2015). β-Aminobutyric acid–induced resistance against root-knot nematodes in Rice is based on increased basal defense. Molecular Plant-Microbe Interactions, 28(5), 519–533. https://doi.org/10.1094/MPMI-09-14-0260-R.
Klose, S., Wu, B. M., Ajwa, H. A., Koike, S. T., & Subbarao, K. V. (2010). Reduced efficacy of rovral and botran to control Sclerotinia minor in lettuce production in the Salinas Valley may be related to accelerated fungicide degradation in soil. Crop Protection, 29(7), 751–756. https://doi.org/10.1016/J.CROPRO.2010.02.015.
Kohn, L. M. (1979). Delimitation of the economically important plant pathogenic Sclerotinia species. Phytopathology, 69(8), 881. https://doi.org/10.1094/Phyto-69-881.
Liang, X., Liberti, D., Li, M., Kim, Y.-T., Hutchens, A., Wilson, R., & Rollins, J. A. (2015). Oxaloacetate acetylhydrolase gene mutants of Sclerotinia sclerotiorum do not accumulate oxalic acid, but do produce limited lesions on host plants. Molecular Plant Pathology, 16(6), 559–571. https://doi.org/10.1111/mpp.12211.
Lim, C., Baek, W., Jung, J., Kim, J.-H., & Lee, S. (2015). Function of ABA in stomatal defense against biotic and drought stresses. International Journal of Molecular Sciences, 16(7), 15251–15270. https://doi.org/10.3390/ijms160715251.
Lim, C. W., Luan, S., & Lee, S. C. (2014). A prominent role for RCAR3-mediated ABA signaling in response to Pseudomonas syringae pv. Tomato DC3000 infection in Arabidopsis. Plant and Cell Physiology, 55(10), 1691–1703. https://doi.org/10.1093/pcp/pcu100.
Llorens, E., Agustí-Brisach, C., González-Hernández, A. I., Troncho, P., Vicedo, B., Yuste, T., et al. (2016). Bioassimilable Sulphur provides effective control of Oidium neolycopersici in tomato, enhancing the plant immune system. Pest Management Science. https://doi.org/10.1002/ps.4419.
Llorens, E., Fernández-Crespo, E., Vicedo, B., Lapeña, L., & García-Agustín, P. (2013). Enhancement of the citrus immune system provides effective resistance against Alternaria brown spot disease. Journal of Plant Physiology, 170(2). https://doi.org/10.1016/j.jplph.2012.09.018.
Llorens, E., García-Agustín, P., & Lapeña, L. (2017). Advances in induced resistance by natural compounds: Towards new options for woody crop protection. Scientia Agricola, 74(1). https://doi.org/10.1590/1678-992x-2016-0012.
McDonald, J. A., Gaston, L. A., Jackson, S. H., Locke, M. A., & Zablotowicz, R. M. (2006). DEGRADATION KINETICS ASSESSMENT FOR THE FUNGICIDE BAS 505 IN INTACT SOIL CORES VERSUS BATCH SOILS. Soil Science, 171(3), 239–248. https://doi.org/10.1097/01.ss.0000187375.38649.5b.
Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., et al. (2011). ROS signaling: The new wave? Trends in Plant Science, 16(6), 300–309. https://doi.org/10.1016/J.TPLANTS.2011.03.007.
Nováková, M., Šašek, V., Dobrev, P. I., Valentová, O., & Burketová, L. (2014). Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum – Reassessing the role of salicylic acid in the interaction with a necrotroph. Plant Physiology and Biochemistry, 80, 308–317. https://doi.org/10.1016/J.PLAPHY.2014.04.019.
Oide, S., Bejai, S., Staal, J., Guan, N., Kaliff, M., & Dixelius, C. (2013). A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. New Phytologist, 200(4), 1187–1199. https://doi.org/10.1111/nph.12436.
Ojaghian, M. R., Wang, L., Cui, Z. q., Yang, C., Zhongyun, T., & Xie, G.-L. (2014). Antifungal and SAR potential of crude extracts derived from neem and ginger against storage carrot rot caused by Sclerotinia sclerotiorum. Industrial Crops and Products, 55, 130–139. https://doi.org/10.1016/J.INDCROP.2014.02.012.
Ortega-Aguilar, B. L., Alarcón, A., & Ferrera-Cerrato, R. (2011). Effect of potassium bicarbonate on fungal growth and sclerotia of Sclerotium cepivorum and its interaction with Trichoderma. Revista mexicana de micologia, (33), 53–61. http://www.scielo.org.mx/pdf/rmm/v33/v33a8.pdf. Accessed 18 January 2018
Padilha, I. Q. M., Pereira, A. V., Rodrigues, O. G., Siqueira-Júnior, J. P., & Pereira, M. d. S. V. (2010). Antimicrobial activity of Mimosa tenuiflora (Willd.) Poir. From Northeast Brazil against clinical isolates of Staphylococcus aureus. Revista Brasileira de Farmacognosia, 20(1), 45–47. https://doi.org/10.1590/S0102-695X2010000100010.
Pane, C., Francese, G., Raimo, F., Mennella, G., & Zaccardelli, M. (2017). Activity of foliar extracts of cultivated eggplants against sclerotinia lettuce drop disease and their phytochemical profiles. European Journal of Plant Pathology, 148(3), 687–697. https://doi.org/10.1007/s10658-016-1126-0.
Pane, C., Fratianni, F., Caputo, M., Parisi, M., Nazzaro, F., & Zaccardelli, M. (2015). Antifungal activity of wild Capsicum foliar extracts containing polyphenols against the phytopathogens Alternaria alternata, Rhizoctonia solani, Sclerotinia minor and Verticillium dahliae. In A. Mendez-Vilas (Ed.), Multidisciplinary approach for studying and combating microbial pathogens (pp. 34–38). Boca Raton: Brown Walker Press.
Pansera, M. R., Pauletti, M., Fedrigo, C. P., Sartori, V. C., Ribeiro, R. T. da S. (2008). Utilization of essential oil and vegetable extracts of Salvia officinalis L. in the control of rot sclerotinia in lettuce. Applied Research & Agrotechnology, 6(2), 83–88. http://revistas.unicentro.br/index.php/repaa/article/view/2248/2176. Accessed 7 December 2017
Paul, P. ., & Sharma, P. . (2002). Azadirachta indica leaf extract induces resistance in barley against leaf stripe disease. Physiological and Molecular Plant Pathology, 61(1), 3–13. https://doi.org/10.1006/PMPP.2002.0412.
Paulert, R., Ebbinghaus, D., Urlass, C., & Moerschbacher, B. M. (2010). Priming of the oxidative burst in rice and wheat cell cultures by ulvan, a polysaccharide from green macroalgae, and enhanced resistance against powdery mildew in wheat and barley plants. Plant Pathology, 59(4), 634–642. https://doi.org/10.1111/j.1365-3059.2010.02300.x.
Gillitzer, P., Martin, A. C., Kantar, M. B., Kauppi, K., Dahlberg, S., Lis, D., et al. (2012). Optimization of screening of native and naturalized plants from Minnesota for antimicrobial activity. Journal of Medicinal Plants Research, 6(6), 938–949. https://doi.org/10.5897/JMPR10.710.
Purdy, L. H. (1979). Sclerotinia sclerotiorum : History, diseases and symptomatology, host range, geographic distribution, and impact. Phytopathology, 69(8), 875. https://doi.org/10.1094/Phyto-69-875.
Saharan, G. S., Mehta, N. (2008). Sclerotinia diseases of crop plants : biology, ecology and disease management. Springer. https://books.google.es/books?id=uvaQCSybm_gC&pg=PA131&lpg=PA131&dq=Dillon-Weston+et+al.,+1946;+Starr+et+al.,+1953&source=bl&ots=Tq-KI4d9HE&sig=1odA6uCgQjCC1AjQouSgmkiCdyA&hl=es&sa=X&ved=0ahUKEwiG8vKI7tLYAhXJPxQKHfruD4wQ6AEIKjAA#v=onepage&q=Dillon-Weston. Accessed 12 January 2018.
Sales, M. D. C., Costa, H. B., Fernandes, P. M. B., Ventura, J. A., & Meira, D. D. (2016). Antifungal activity of plant extracts with potential to control plant pathogens in pineapple. Asian Pacific Journal of Tropical Biomedicine, 6(1), 26–31. https://doi.org/10.1016/J.APJTB.2015.09.026.
Sanderson, K., Bariccatti, R. A., Primieri, C., Viana, H., Viecelli, C. A., Guilherme, H., & Junior, B. (2013). Allelopathic influence of the aqueous extract of jatropha on lettuce (Lactuca sativa var. Grand Rapids) germination and development. Journal of Food, Agriculture & Environment Journal of Food Agriculture & Environment, 1111(11), 641–643. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.659.1607&rep=rep1&type=pdf. Accessed 12 January 2018
Shrestha, A., Sultana, R., Chae, J.-C., Kim, K., & Lee, K.-J. (2015). Bacillus thuringiensis C25 which is rich in cell wall degrading enzymes efficiently controls lettuce drop caused by Sclerotinia minor. European Journal of Plant Pathology, 142(3), 577–589. https://doi.org/10.1007/s10658-015-0636-5.
Smolińska, U., & Kowalska, B. (2018). Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum –– A review. Journal of Plant Pathology, 100(1), 1–12. https://doi.org/10.1007/s42161-018-0023-0.
Steel, R. G. D., Torrie, J. H. (1986). Bioestadistica: principios y procedimientos (2nd ed.). Mexico: McGraw-Hill. http://www.urbe.edu/UDWLibrary/InfoBook.do?id=5221.
Tian, J., Ban, X., Zeng, H., Huang, B., He, J., & Wang, Y. (2011). In vitro and in vivo activity of essential oil from dill (Anethum graveolens L.) against fungal spoilage of cherry tomatoes. Food Control, 22(12), 1992–1999. https://doi.org/10.1016/J.FOODCONT.2011.05.018.
Vicedo, B., Flors, V., Leyva, M. D., Finiti, I., Kravchuk, Z., Real, M. D., et al. (2009). Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Molecular Plant-Microbe Interactions, 22(11), 1455–1465. https://doi.org/10.1094/mpmi-22-11-1455.
Voigt, C. A. (2016). Cellulose/callose glucan networks: The key to powdery mildew resistance in plants? New Phytologist, 212(2), 303–305. https://doi.org/10.1111/nph.14198.
Wang, H., Wang, J., Peng, X., Zhou, P., Bai, N., Meng, J., & Deng, X. (2014). Control efficacy against rice sheath blight of Platycladus orientalis extract and its antifungal active compounds. European Journal of Plant Pathology, 140(3), 515–525. https://doi.org/10.1007/s10658-014-0485-7.
Williams, B., Kabbage, M., Kim, H.-J., Britt, R., & Dickman, M. B. (2011). Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathogens, 7(6), e1002107. https://doi.org/10.1371/journal.ppat.1002107.
Wojtaszek, P. (1997). Oxidative burst: an early plant response to pathogen infection. The Biochemical journal, 322 ( Pt 3) (Pt 3), 681–92. http://www.ncbi.nlm.nih.gov/pubmed/9148737. Accessed 7 December 2017
Acknowledgements
This research was financially supported by the ‘Instituto Valenciano de Competitividad Empresarial’ (IVACE) Ref. IFINOA/2014/46 and the Spanish Ministry of Science and Innovation (AGL2013-49023-C3-2-R). Ana I. González-Hernández is the holder of a fellowship by the “Programa de formació del personal investigador (PREDOC/2016/27)” and C. Agustí-Brisach is the holder of a ‘Juan de la Cierva-Incorporación’ postdoctoral fellowship from MINECO. The authors are grateful to the ‘Serveis Centrals d’Instrumentació Científica’ (SCIC) from ‘Universitat Jaume I’ (UJI, Castellón, Spain).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Authors declared that this manuscript has not published elsewhere. All the authors have read very carefully and approved current version of this manuscript. All authors also declared that the data or images have not manipulated.
Conflicts of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This research is focused on the mechanism of action of botanical extracts against a plant pathogenic fungus. This article does not contain any experiments with human participants or animals.
Informed consent
Please be informed that authors are satisfied to publish this work in European Journal of Plant Pathology.
Rights and permissions
About this article
Cite this article
Llorens, E., Mateu, M., González-Hernández, A.I. et al. Extract of Mimosa tenuiflora and Quercus robur as potential eco-friendly management tool against Sclerotinia sclerotiorum in Lactuca sativa enhancing the natural plant defences. Eur J Plant Pathol 153, 1105–1118 (2019). https://doi.org/10.1007/s10658-018-01629-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-018-01629-3