Cell-wall degrading enzymes for the control of Meloidogyne javanica
Bruno C. Aita, Breno B. Heinz, Eliana A. Alves, Ethiane T. Mezadri, Stefani S. Spannemberg, Izabelle S. Romagna, Patricia A. Karsburg, Emanuele Junges, Raquel C. Kuhn, Marcio A. Mazutti
Abstract
The potential of cell-wall degrading enzymes (chitinase, β-1,3 glucanase, endo-cellulase and exocellulase) in the control of M. javanica in vitro and in vivo was investigated in this study. The enzymes were produced by solid-state fermentation using Beauveria bassiana, Trichoderma harzianum and Metarhizium anisopliae, microorganisms that are used in the biological control of agricultural pests. The bioproducts were efficient in the treatments in vitro, presenting high indexes of egg hatching inhibition (66.7-87.0%) and mortality of juveniles (40.0-90.0%). The bioproduct containing enzymes from B. bassiana presented the most promising results. In vivo treatments with all bioproducts on lettuce and tomato cultures during initial stages of plant development demonstrated excellent nematicidal effects in relation to the water-treated control. On lettuce, final egg counts and juveniles in the control treatment were 141 and 452% higher than in treatments containing bioproducts, respectively. The index of penetration of M. javanica on tomato roots was 348% higher in the control treatment than in the treatments using bioproducts. The bioproducts evaluated in this study were efficient in the control of nematodes both in treatments in vitro and in vivo. The results obtained open a new perspective for the use of bioproducts containing cell-wall degrading enzymes for the control of nematodes in agriculture.
References
Aballay, E., Prodan, S., Zamorano, A., & Castaneda-Alvarez, C. (2017). Nematicidal effect of rhizobacteria on plant-parasitic nematodes associated with vineyards. World Journal of Microbiology & Biotechnology, 33(7), 131. http://dx.doi.org/10.1007/s11274-017-2303-9. PMid:28585175.
Abd-Elgawad, M. M. M., & Askary, T. H. (2018). Fungal and bacterial nematicides in integrated nematode management strategies. Egyptian Journal of Biological Pest Control, 28(1), 74. http://dx.doi.org/10.1186/s41938-018-0080-x.
Berini, F., Katz, C., Gruzdev, N., Casartelli, M., Tettamanti, G., & Marinelli, F. (2018). Microbial and viral chitinases: Attractive biopesticides for integrated pest management. Biotechnology Advances, 36(3), 818-838. http://dx.doi.org/10.1016/j.biotechadv.2018.01.002. PMid:29305895.
Bird, A. F., & Bird, J. (1991). The structure of nematodes (2nd ed.). San Diego: Academic Press.
Brasil, Ministério da Agricultura Pecuária e Abastecimento. (2019). Agrofit: sistema de agrotóxicos fitossanitários. Available online: http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons
Bybd, J. D. W., Kirkpatrick, J., & Barker, K. R. (1983). An improved technique for clearing and staining plant tissues for detection of nematodes. Journal of Nematology, 15(1), 142-143. PMid:19295781.
Castaneda-Alvarez, C., Prodan, S., Rosales, I. M., & Aballay, E. (2016). Exoenzymes and metabolites related to the nematicidal effect of rhizobacteria on Xiphinema index Thorne & Allen. Journal of Applied Microbiology, 120(2), 413-424. http://dx.doi.org/10.1111/jam.12987. PMid:26541369.
Chandrasekaran, R., Revathi, K., Nisha, S., Kirubakaran, S. A., Sathish-Narayanan, S., & Senthil-Nathan, S. (2012). Physiological effect of chitinase purified from Bacillus subtilis against the tobacco cutworm Spodoptera litura Fab. Pesticide Biochemistry and Physiology, 104(1), 65-71. http://dx.doi.org/10.1016/j.pestbp.2012.07.002.
de Las Rivas, B., Rodríguez, H., Anguita, J., & Muñoz, R. (2019). Bacterial tannases: classification and biochemical properties. Applied Microbiology and Biotechnology, 103(2), 603-623. http://dx.doi.org/10.1007/s00253-018-9519-y. PMid:30460533.
Devi, G., & Bora, L. C. (2018). Effect of some biocontrol agents against root-knot nematode (Meloidogyne incognita race2). International Journal of Environment Agriculture and Biotechnology, 3(5), 1748-1755. http://dx.doi.org/10.22161/ijeab/3.5.23.
El-Katatny, M. H., Gudelj, M., Robra, K. H., Elnaghy, M. A., & Gübitz, G. M. (2001). Characterization of a chitinase and an endo-β1,3-glucanase from Trichoderma harzianum Rifai T24 involved in control of the phytopathogen Sclerotium rolfsii. Applied Microbiology and Biotechnology, 56(1-2), 137-143. http://dx.doi.org/10.1007/s002530100646. PMid:11499921.
Engelbrecht, G., Horak, I., Jansen van Rensburg, P. J., & Claassens, S. (2018). Bacillus-based bionematicides: Development, modes of action and commercialisation. Biocontrol Science and Technology, 28(7), 629-653. http://dx.doi.org/10.1080/09583157.2018.146 9000.
Ghose, T. K. (1987). Measurement of cellulase activities. Pure and Applied Chemistry, 59(2), 257-268. http://dx.doi.org/10.1351/pac198759020257.
Gortari, M. C., & Hours, R. A. (2008). Fungal chitinases and their biological role in the antagonism onto nematode eggs: a review. Mycological Progress, 7(4), 221-238. http://dx.doi.org/10.1007/s11557-008-0571-3.
Graham, M. H., Haynes, R. J., & Meyer, J. H. (2002). Soil organic matter content and soil quality: effects of fertilizer applications, burning and trash retention on a long-term sugarcane experiment in South Africa. Soil Biology & Biochemistry, 34(1), 93-102. http://dx.doi.org/10.1016/S0038-0717(01)00160-2.
Hashem, M., & Abo-Elyousr, K. A. (2011). Management of the root-knot nematode Meloidogyne incognita on tomato with combinations of different biocontrol organisms. Crop Protection, 30(3), 285-292. http://dx.doi.org/10.1016/j.cropro.2010.12.009.
Hussey, R. S., & Barker, K. R. (1973). A comparasion of methods for collection inocula of Meloidogyne spp., including a new technique. The Plant Disease Reporter, 57, 1025-1028.
Jiang, C., Song, J., Cong, H., Zhang, J., & Yang, Q. (2017). Expression and Characterization of a Novel Antifungal Exo-β1,3-glucanase from Chaetomium cupreum. Applied Biochemistry and Biotechnology, 182(1), 261-275. http://dx.doi.org/10.1007/s12010-016-2325-z. PMid:27854040.
Kamala, T., & Indira, S. (2011). Evaluation of indigenous Trichoderma isolates from Manipur as biocontrol agent against Pythium aphanidermatum on common beans. 3 Biotech, 1(4), 217-225. http://dx.doi.org/10.1007/s13205-011-0027-3. PMid:22558540.
Khan, A., Williams, K. L., & Nevalainen, H. K. M. (2004). Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biological Control, 31(3), 346-352. http://dx.doi.org/10.1016/j.biocontrol.2004.07.011.
Kim, K., Yang, Y., & Kim, J. (2003). Purification and Characterization of Chitinase from Streptomyces sp. M-20. Journal of Biochemistry and Molecular Biology, 36(2), 185-189. http://dx.doi.org/10.5483/BMBRep.2003.36.2.185. PMid:12689517.
Lee, Y. S., & Kim, K. Y. (2015). Statistical optimization of medium components for chitinase production by Pseudomonasfluorescens strain HN1205: Role of chitinase on egg hatching inhibition of rootknot nematode. Biotechnology, Biotechnological Equipment, 29(3), 470-478. http://dx.doi.org/10.1080/13102818.2015.1010702.
Luquini, L., Barbosa, D., Haddad, F., Ferreira, C. F., & Amorim, E. P. (2019). Nematode survey and biochemical characterization of Meloidogyne spp. in a main banana production area in Brazil. Crop Protection (Guildford, Surrey), 117, 94-99. http://dx.doi.org/10.1016/j.cropro.2018.11.018.
Patil, N. S., & Jadhav, J. P. (2015). Significance of Penicillium ochrochloron chitinase as a biocontrol agent against pest Helicoverpa armigera. Chemosphere, 128, 231-235. http://dx.doi.org/10.1016/j.chemosphere.2015.01.038. PMid:25723715.
Pitcher, R. S., & Flegg, J. J. M. (1968). An improved final separation sieve for the extraction of plant-parasitic nematodes from soil debris. Nematologica, 14(1), 123-127. http://dx.doi.org/10.1163/187529268X00705.
Qualhato, T. F., Lopes, F. A., Steindorff, A. S., Brandão, R. S., Jesuino, R. S., & Ulhoa, C. J. (2013). Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnology Letters, 35(9), 1461-1468. http://dx.doi.org/10.1007/s10529-013-1225-3. PMid:23690037.
Resquín-Romero, G., Garrido-Jurado, I., & Quesada-Moraga, E. (2016). Combined use of entomopathogenic fungi and their extracts for the control of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Biological Control, 92, 101-110. http://dx.doi.org/10.1016/j.biocontrol.2015.10.007.
Rocha, T. L., Soll, C. B., Boughton, B. A., Silva, T. S., Oldach, K., Firmino, A. A. P., Callahan, D. L., Sheedy, J., Silveira, E. R., Carneiro, R. M. D. G., Silva, L. P., Polez, V. L. P., Pelegrini, P. B., Bacic, A., Grossi-de-Sa, M. F., & Roessner, U. (2017). Prospection and identification of nematotoxic compounds from Canavalia ensiformis seeds effective in the control of the root knot nematode Meloidogyne incognita. Biotechnology Research and Innovation, 1(1), 87-100. http://dx.doi.org/10.1016/j.biori.2017.10.003.
Ruiu, L. (2018). Microbial Biopesticides in Agroecosystems. Agronomy, 8(11), 235. http://dx.doi.org/10.3390/agronomy8110235.
Senol, M., Nadaroglu, H., Dikbas, N., & Kotan, R. (2014). Purification of Chitinase enzymes from Bacillus subtilis bacteria TV-125, investigation of kinetic properties and antifungal activity against Fusarium culmorum. Annals of Clinical Microbiology and Antimicrobials, 13(1), 35. http://dx.doi.org/10.1186/s12941-014-0035-3. PMid:25112904.
Strasser, H., Vey, A., & Butt, T. M. (2000). Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species? Biocontrol Science and Technology, 10(6), 717-735. http://dx.doi.org/10.1080/09583150020011690.
Treichel, H., Oliveira, D., Mazutti, M. A., Di Luccio, M., & Oliveira, J. V. (2010). A review on microbial lipases production. Food and Bioprocess Technology, 3(2), 182-196. http://dx.doi.org/10.1007/s11947-009-0202-2.
Van Nguyen, N., Kim, Y.-J., Oh, K.-T., Jung, W.-J., & Park, R.-D. (2007). The role of chitinase from Lecanicillium antillanum B-3 in parasitism to root-knot nematode Meloidogyne incognita eggs. Biocontrol Science and Technology, 17(10), 1047-1058. http://dx.doi.org/10.1080/09583150701668658.
Wang, B., Liu, X., Wu, W., Liu, X., & Li, S. (2009). Purification, characterization and gene cloning of an alkaline serine protease from a highly virulent strain of the nematode-endoparasitic fungus Hirsutella rhossiliensis. Microbiological Research, 164(6), 665-673. http://dx.doi.org/10.1016/j.micres.2009.01.003. PMid:19303270.
Wang, J., Wang, J., Liu, F., & Pan, C. (2010). Enhancing the virulence of Paecilomyces lilacinus against Meloidogyne incognita eggs by overexpression of a serine protease. Biotechnology Letters, 32(8), 1159-1166. http://dx.doi.org/10.1007/s10529-010-0278-9. PMid:20473777.
Wang, R. B., Yang, J. K., Lin, C., Zhang, Y., & Zhang, K. Q. (2006). Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Dactylella shizishanna. Letters in Applied Microbiology, 42(6), 589-594. http://dx.doi.org/10.1111/j.1472-765X.2006.01908.x. PMid:16706897.
Yang, J., Liang, L., Li, J., & Zhang, K. (2013). Nematicidal enzymes from microorganisms and their applications. Applied Microbiology and Biotechnology, 97(16), 7081-7095. http://dx.doi.org/10.1007/s00253-013-5045-0. PMid:23832084.
Yu, W. Q., Zheng, G. P., Qiu, D. W., Yan, F. C., Liu, W. Z., & Liu, W. X. (2019). Paenibacillus terrae NK3-4: A potential biocontrol agent that produces β-1,3-glucanase. Biological Control, 129, 92-101. http://dx.doi.org/10.1016/j.biocontrol.2018.09.019.
Yue, X. Y., Zhang, B., Jiang, D. D., Liu, Y. J., & Niu, T. G. (2011). Separation and purification of a keratinase as pesticide against root-knot nematodes. World Journal of Microbiology & Biotechnology, 27(9), 2147-2153. http://dx.doi.org/10.1007/s11274-011-0680-z.
Zhao, D., Liu, B., Wang, Y., Zhu, X., Duan, Y., & Chen, L. (2013). Screening for nematicidal activities of Beauveria bassiana and associated fungus using culture filtrate. African Journal of Microbiological Research, 7(11), 974-978.
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