Inhibidores de proteasas de soya incrementan la toxicidad de Bacillus thuringiensis subs. israelensis contra Hypothenemus hampei

Autores/as

DOI:

https://doi.org/10.15517/am.v31i2.36573

Palabras clave:

control biológico, toxinas bacterianas, harina de soya, inhibidos de proteasas, sinergismo

Resumen

Introducción. La broca del café (Hypothenemus hampei, CBB) es una de las plagas más devastadoras en plantaciones de café alrededor del mundo. Aunque CBB es susceptible al efecto de las δ-endotoxinas del Bacillus thuringiensis subs. israelensis (Bti) a nivel de laboratorio, la eficacia de este método de control es deficiente en campo, posiblemente debido a la inactivación ocasionada por proteasas digestivas diferentes a las requeridas para la activación de las protoxinas. Objetivo. Determinar si la incorporación de un extracto de harina de soya con inhibidores de proteasas (PI) mezclado con cristales y esporas de Bti (Bti-sc) en una dieta artifical, podría mejorar la toxicidad de Bti contra CBB. Materiales y métodos. Este estudio se realizó en San José, Costa Rica entre 2012 y 2013. Se expuso un conjunto de insectos hembras adultas de CBB a una mezcla que incluyó diferentes concentraciones del extracto de soya parcialmente purificado con PI activo y un liofilizado de Bti-sc, y fueron evaluadas mediante un bioensayo en dieta artificial para estimar la concentración subletal (CL50). Los resultados de mortalidad se validaron mediante observación del intestino medio diseccionado, cuya ultraestructura se analizó mediante microscopía electrónica de transmisión. Resultados. El extracto de soya degradó parcialmente el complejo Bti-sc, redujo la CL50 en casi cuatro veces (de 1,135 a 0,315 µg µl-1) y potenció la mortalidad de CBB de manera concentración-dependiente. Los análisis histológicos del intestino medio confirmaron este efecto sinérgico, dado que se visualizaron daños severos en el epitelio intestinal de CBB expuestos a Bti-sc + PI comparado con Bti-sc solo. Conclusiones. La combinación del extracto de soya enriquecido con PI y Bti-sc potenció la letalidad sobre CBB, que se confirmó por el colapso intestinal. La harina de soya es un suplemento económico que podría aumentar la efectividad de Bti para controlar CBB y retrasar el desarrollo de resistencia biológica.

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Acuña-González, P., y W. Betanco Velásquez. 2007. Evaluación de la incidencia natural de Beauveria bassiana (Bals) Vuill, sobre Hypothenemus hampei (Ferrari) y Leucoptera coffeella (Guérin-Méneville) en el cultivo de café en dos zonas cafetaleras de Nicaragua. Tesis Diploma, Universidad Nacional Agraria, Managua, NIC.

Anderson, R.L., and W.J. Wolf. 1995. Compositional changes in trypsin inhibitors, phytic acid, saponins and isoflavones related to soybean processing. J. Nutr. 125:581S-588S. doi:10.1093/jn/125.3_Suppl.581S

Aristizábal, L.F., M. Jiménez, A.E. Bustillo, H.I. Trujillo, and S.P. Arthurs. 2015. Monitoring coffee berry borer, Hypothenemus hampei (Coleoptera: Curculionidae), populations with alcohol-baited funnel traps in coffee farms in Colombia. FL Entomol. 98:381-383. doi:10.1653/024.098.0165

Aristizábal, L.F., S. Shriner, R. Hollingsworth, and S. Arthurs. 2017. Flight activity and field infestation relationships for coffee berry borer in commercial coffee plantations in Kona and Kau districts, Hawaii. J. Econ. Entomol. 110:2421–2427. doi:10.1093/jee/tox215

Belayneh-Mulaw, T., C.P. Kubicek, and I.S. Druzhinina. 2010. The rhizosphere of Coffea arabica in its native highland forests of Ethiopia provides a niche for a distinguished diversity of Trichoderma. Diversity 2:527-549. doi:10.3390/d2040527

Cantor, F., V.L.R.M. Benassi, e C.J. Fanton. 2001. Broca-do-café, Hypothenemus hampei (Coleoptera: Scolytidae). Em: E. Ferrera et al., editores, Histórico e impacto das pragas introduzidas no Brasil. Holos, São Paulo, BRA. p. 99-105.

Cárdenas, S.I. 2007. Caracterización morfológica y agronómica de la colección núcleo de café (Coffea arabica L.) del CATIE. Tesis MSc., CATIE, Turrialba, CRI.

Constantino, L.M., L. Navarro, A. Berrio, F.E. Acevedo, D. Rubio, y P. Benavides. 2011. Aspectos biológicos, morfológicos y genéticos de Hypothenemus obscurus e Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae). Rev. Colomb. Entomol. 37:173-182.

Cotabarren, J., D. Lufrano, M.G. Parisi, and W.D. Obregón. 2020. Biotechnological, biomedical, and agronomical applications of plant protease inhibitors with high stability: A systematic review. Plant Sci. 292:110398. doi:10.1016/j.plantsci.2019.110398

De-la-Rosa, W., M. Figueroa, and J. Ibarra. 2005. Selection of Bacillus thuringiensis strains native to Mexico active against the coffee berry borer Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae). Vedalia 12:3-9.

de-Oliveira, C.F.R., I.M. Vasconcelos, R. Aparicio, M.D.G.M. Freire, P.A. Baldasso, S. Marangoni, and M.L.R. Macedo. 2012. Purification and biochemical properties of a Kunitz-type trypsin inhibitor from Entada acaciifolia (Benth.) seeds. Proc. Biochem. 47:929-935. doi:10.1016/j.procbio.2012.02.022

El-latif, A.O.A. 2015. Protease purification and characterization of a serine protease inhibitor from Egyptian varieties of soybean seeds and its efficacy against Spodoptera littoralis. J. Plant Prot. Res. 55:16-25. doi:10.1515/jppr-2015-0003

Erlanger, B.F., N. Kokowsky, and W. Cohen. 1961. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95:271-278. doi:10.1016/0003-9861(61)90145-X

Fabrick, J., C. Behnke, T. Czapla, K. Bala, A.G. Rao, K.J. Kramer, and G.R. Reeck. 2002. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae). Insect Biochem. Mol. Biol. 32:405-415. doi:10.1016/S0965-1748(01)00117-5

Finney, D.J., and W.L. Stevens. 1948. A table for the calculation of working probits and weights in probit analysis. Biometrika 35:191-201. doi:10.1093/biomet/35.1-2.191

Franco, O.L., S.C. Dias, C.P. Magalhães, A.C.S. Monteiro, C. Bloch, F.R. Melo, O.B. Oliveira-Neto, R.G. Monnerat, and M.F. Grossi-de-Sá. 2004. Effects of soybean Kunitz trypsin inhibitor on the cotton boll weevil (Anthonomus grandis). Phytochemistry 65:81-89. doi:10.1016/j.phytochem.2003.09.010

García-Carreño, F.L., and N.F. Haard. 1993. Characterization of proteinase classes in langostilla (Pleuroncodes planipes) and crayfish (Pacifastacus astacus) extracts. J. Food Biochem. 17:97-113. doi:10.1111/j.1745-4514.1993.tb00864.x

Ghodke, A.B., S.G. Chavan, B.V. Sonawane, and A.A. Bharose. 2013. Isolation and in vitro identification of proteinase inhibitors from soybean seeds inhibiting Helicoverpa gut proteases. J. Plant Interact. 8:170-178. doi:10.1080/17429145.2012.668952

Gillman, J.D., W.S. Kim, and H.B. Krishnan. 2015. Identification of a new soybean Kunitz trypsin inhibitor mutation and its effect on Bowman-Birk protease inhibitor content in soybean seed. J. Agric. Food Chem. 63:1352-1359. doi:10.1021/jf505220p

González, V. 2019. Costa Rica: Coffee annual: Coffee production and trade. Annual report. USDA, USA. https://gain.fas.usda.gov/Recent%20GAIN%20Publications/Coffee%20Annual_San%20Jose_Costa%20Rica_5-15-2019.pdf (accessed Sep. 29, 2019).

Gu, C., X. Song, L. Zhao, S. Pan, and G. Qin. 2014. Purification and characterization of Bowman-Birk trypsin inhibitor from soybean. J. Food Nutr. Res. 2:546-550. doi:10.12691/jfnr-2-9-3

Guedidi, S., Y. Yurekli, A. Deratani, P. Déjardin, C. Innocent, S.A. Altinkaya, S. Roudesli, and A. Yemenicioglu. 2010. Effect of enzyme location on activity and stability of trypsin and urease immobilized on porous membranes by using layer-by-layer self-assembly of polyelectrolyte. J. Membr. Sci. 365:59-67. doi:10.1016/j.memsci.2010.08.042

Gujar, T., V. Kalia, A. Kumari, and T.V. Prasad. 2004. Potentiation of insecticidal activity of Bacillus thuringiensis subsp. kurstaki HD-1 by proteinase inhibitors in the American bollworm, Helicoverpa armigera (Hübner). Indian J. Exp. Biol. 42(2):157-163.

Hernández-Soto, A., M.C. Del Rincón-Castro, A.M. Espinoza, and J.E. Ibarra. 2009. Parasporal body formation via overexpression of the Cry10Aa toxin of Bacillus thuringiensis subsp. israelensis, and Cry10Aa-Cyt1Aa synergism. Appl. Environ. Microbiol. 75:4661-4667. doi:10.1128/AEM.00409-09

Jiménez, A.J. 2009. As enzimas presentes no trato digestivo dos insetos: um alvo susceptível de inhibição. Tese Dou., Universidade de Brasília, Brasilia, BRA.

Jouzani, G.S., E. Valijanian, and R. Sharafi. 2017. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl. Microbiol. Biotechnol. 101:2691-2711. doi:10.1007/s00253-017-8175-y

Kakade, M.L., J.J. Rackis, J.E. McGhee, G. Puski, and R.S. Usda. 1974. Determination of trypsin inhibitor activity of soy products: a collaborative analysis of an improved procedure. Cereal Chem. 51:376-381.

Kirouac, M., V. Vachon, D. Quievy, J.L. Schwartz, and R. Laprade. 2006. Protease inhibitors fail to prevent pore formation by the activated Bacillus thuringiensis toxin Cry1Aa in insect brush border membrane vesicles. Appl. Environ. Microbiol. 72:506-515. doi:10.1128/AEM.72.1.506-515.2006

Kuhar, K., R. Kansal, B. Subrahmanyam, K.R. Koundal, K. Miglani, and V.K. Gupta. 2013. A Bowman–Birk protease inhibitor with antifeedant and antifungal activity from Dolichos biflorus. Acta Physiol. Plant. 35:1887-1903. doi:10.1007/s11738-013-1227-8

Lecadet, M.M., M.O. Blondel, and J. Ribier. 1980. Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber. Microbiol. 121:203-212. doi:10.1099/00221287-121-1-203

Li, J., and H.A. Chase. 2010. Applications of membrane techniques for purification of natural products. Biotechnol. Lett. 32:601-608. doi:10.1007/s10529-009-0199-7

Lomate, P.R., and V.K. Hivrale. 2013. Effect of Bacillus thuringiensis (Bt) Cry1Ac toxin and protease inhibitor on growth and development of Helicoverpa armigera (Hübner). Pest. Biochem. Physiol. 105(2):77-83. doi:10.1016/j.pestbp.2013.01.002

López-Pazos, S.A., J.E. Cortázar-Gómez, and J.A. Cerón-Salamanca. 2009. Cry1B and Cry3A are active against Hypothenemus hampei Ferrari (Coleoptera: Scolytidae). J. Invertebr. Pathol. 101:242-245. doi:10.1016/j.jip.2009.05.011

Macedo, M.L.R, Md. Freire, O.L. Franco, L. Migliolo, and C.F. de-Oliveira. 2011. Practical and theoretical characterization of Inga laurina Kunitz inhibitor on the control of Homalinotus coriaceus. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 158:164-172. doi:10.1016/j.cbpb.2010.11.005

MacIntosh, S.C., G.M. Kishore, F.J. Perlak, P.G. Marrone, T.B. Stone, S.R. Sims, and R.L. Fuchs. 1990. Potentiation of Bacillus thuringiensis insecticidal activity by serine protease inhibitors. J. Agric. Food Chem. 38:1145-1152. doi:10.1021/jf00094a051

Mansour, S.A., M.S. Foda, and A.R. Aly. 2012. Mosquitocidal activity of two Bacillus bacterial endotoxins combined with plant oils and conventional insecticides. Ind. Crop Prod. 35:44-52. doi:10.1016/j.indcrop.2011.06.001

McDonald, K. 2007. Cryopreparation methods for electron microscopy of selected model systems. In: J.R. McIntosh, editor, Cellular electron microscopy. Academic Press, Elsiever, San Diego, CA, USA. p. 23-56. doi:10.1016/S0091-679X(06)79002-1

Méndez-López, I., R. Basurto-Ríos, and J.E. Ibarra. 2003. Bacillus thuringiensis serovar israelensis is highly toxic to the coffee berry borer, Hypothenemus hampei Ferr. (Coleoptera: Scolytidae). FEMS Microbiol. Lett. 226:73-77. doi:10.1016/S0378-1097(03)00557-3

Molina, D., A. Blanco-Labra, y H. Zamora. 2011. Inhibidores de proteasas de plantas efectivos contra las aspártico proteasas de Hypothenemus hampei. Rev. Colomb. Entomol. 37:183-191.

Oliveira, C.M., A.M. Auad, S.M. Mendes, and M.R. Frizzas. 2013. Economic impact of exotic insect pests in Brazilian agriculture. J. Appl. Entomol. 137:1-15. doi:10.1111/jen.12018

Oppert, B., T.D. Morgan, and K.J. Kramer. 2011. Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors against coleopteran storage pests. Pest Manag. Sci. 67:568-573. doi:10.1002/ps.2099

Pan, D., A.P. Hill, A. Kashou, K.A. Wilson, and A. Tan-Wilson. 2011. Electrophoretic transfer protein zymography. Anal. Biochem. 411:277-283. doi:10.1016/j.ab.2011.01.015

Panchal, B.M., and M. Kachole. 2012. Identification of potent inhibitors of Chilo partellus (Swinhoe) (Lepidoptera: Pyralidae) gut proteinase from plant gum PIs. Int. J. Sci. Technol. 1:662-670.

Pardey, A.E.B. 2006. Una revisión sobre la broca del café, Hypothenemus hampei (coleoptera: Curculionidae: Scolytinae), en Colombia. Rev. Colomb. Entomol. 32:101-116.

Perić, V., M. Srebrić, L. Jankuloski, M. Jankulovska, S. Žilić, V. Kandić, and S. Mladenović-Drinić. 2009. The effects of nitrogen on protein, oil and trypsin inhibitor content of soybean. Genetika 41:137-144. doi:10.2298/GENSR0902137P

Portilla, R.M., y D. Streett. 2006. Nuevas técnicas de producción masiva automatizada de Hypothenemus hampei sobre la dieta artificial Cenibroca modificada. Cenicafé 57(1):37-50.

Rojas, M. 2012. Manejo sostenible de la broca del café (Hypothenemus hampei) mediante poda sistemática del cafeto en Costa Rica. Agron. Costarricense 36(2):71-79.

Roosta, H.R., T. Javadi, and F. Nazari. 2011. Isolation and characterization of trypsin inhibitors (Kunitz soybean trypsin inhibitor, Bowman-Birk inhibitor) in soybean. Adv. Environ. Biol. 5:145-153.

Rosenheim, J.A., and M.A. Hoy. 1989. Confidence intervals for the Abbott’s formula correction of bioassay data for control response. J. Econ. Entomol. 82:331-335. doi:10.1093/jee/82.2.331

Ruan, J., J. Yan, S. Hou, H. Chen, Q. Wu, and X. Han. 2015. Expression and purification of the trypsin inhibitor from tartary buckwheat in Pichia pastoris and its novel toxic effect on Mamestra brassicae larvae. Mol. Biol. Rep. 42:209-216. doi:10.1007/s11033-014-3760-y

Schünemann, R., N. Knaak, and L. Fiuza. 2014. Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean culture. ISRN Microbiol. 2014:135675. doi:10.1155/2014/135675

Shamim, M., N.A. Khan, and K.N. Singh. 2011. Inhibition of midgut protease of yellow stem borer (Scirpophaga incertulas) by cysteine protease-like inhibitor from mature jackfruit (Artocarpus heterophyllus) seed. Acta Physiol. Plant. 33:2249-2257. doi:10.1007/s11738-011-0764-2

Shamsi, T.N., R. Parveen, A. Ahmad, R.R. Samal, S. Kumar, and S. Fatima. 2018. Inhibition of gut proteases and development of dengue vector, Aedes aegypti by Allium sativum protease inhibitor. Acta Ecol. Sin. 38:325-328. doi:10.1016/j.chnaes.2018.01.002

Shamsi, T.N., R. Parveen, M. Amir, M.A. Baig, M.I. Qureshi, S. Ali, and S. Fatima. 2016. Allium sativum protease inhibitor: a novel Kunitz trypsin inhibitor from garlic is a new comrade of the serpin family (EA Permyakov, Ed.). PLoS One 11(11):e0165572. doi:10.1371/journal.pone.0165572

Singh, S., A. Singh, S. Kumar, P. Mittal, and I.K. Singh. 2018. Protease inhibitors: recent advancement in its usage as a potential biocontrol agent for insect pest management. Insect Sci. 27:186-201. doi:10.1111/1744-7917.12641

Sriket, C., S. Benjakul, W. Visessanguan, and K. Hara. 2011. Effect of legume seed extracts on the inhibition of proteolytic activity and muscle degradation of fresh water prawn (Macrobrachium rosenbergii). Food Chem. 129:1093-1099. doi:10.1016/j.foodchem.2011.05.080

Suckling, D.M., L.D. Stringer, A.E. Stephens, B. Woods, D.G. Williams, G. Baker, and A.M. El-Sayed. 2014. From integrated pest management to integrated pest eradication: technologies and future needs. Pest Manag. Sci. 70:179-189. doi:10.1002/ps.3670.

Valencia, A., and J. Arboleda. 2005. Digestion of the inhibition αAI by Hypothenemus hampei aspartic proteinases. Rev. Colomb. Entomol. 31:117-121.

Valerio-Oviedo, A. 2006. Evaluación de la incorporación de diferentes fungicidas y dosis en dietas artificiales para la reproducción de la broca de café con miras a la multiplicación de sus parasitoides bajo condiciones controladas. Tesis Bach., Instituto Tecnológico de Costa Rica, Cartago, CRI.

Vasudev, A., and S. K. Sohal. 2016. Partially purified Glycine max proteinase inhibitors: potential bioactive compounds against tobacco cutworm, Spodoptera litura (Fabricius, 1775) (Lepidoptera: Noctuidae). Turk. J. Zool. 40:379-387. doi:10.3906/zoo-1508-20

Vega, F., J. Jaramillo, A. Castillo, and F. Infante. 2009. The coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae): a short review, with recent findings and future research directions. Terr. Arthropod. Rev. 2:129-147. doi:10.1163/187498209X12525675906031

Vidal-Quist, J.C., P. Castañera, and J. González-Cabrera. 2010. Cyt1Aa protein from Bacillus thuringiensis (Berliner) serovar israelensis is active against the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Pest Manag. Sci. 66:949-955. doi:10.1002/ps.1965

Vorlová, L. 2011. Important minor soybens proteins: soybean allergens and enzymes inhibitors. In: H. El-Shemy, editor, Soybean and health. InTech, Brno, CZE. p. 425-432. doi:10.5772/1007

Wei-Salas, S., y A. Durán-Quirós. 2015. Caracterización del uso del suelo en las principales áreas agrícolas de la gran área metropolitana (GAM) de Costa Rica. Agron. Costarricense 39(1):149-160.

Zahiri, N.S., and M.S. Mulla, 2005. Non-larvicidal effects of Bacillus thuringiensis israelensis and Bacillus sphaericus on oviposition and adult mortality of Culex quinquefasciatus Say (Diptera: Culicidae). J. Vector Ecol. 30:155-162.

Zhao, A., Y. Li, C. Leng, P. Wang, and Y. Li. 2019. Inhibitory effect of protease inhibitors on larval midgut protease activities and the performance of Plutella xylostella (Lepidoptera: Plutellidae). Front Physiol. 9:1963. doi:10.3389/fphys.2018.01963

Zhu-Salzman, K., and R. Zeng. 2015. Insect response to plant defensive protease inhibitors. Ann. Rev. Entomol. 60:233-252. doi:10.1146/annurev-ento-010814-020816

Zibaee, I., A.R. Bandani, J.J. Sendi, R. Talaei-Hassanloei, and B. Kouchaki. 2010. Effects of Bacillus thuringiensis var. kurstaki and medicinal plants on Hyphantria cunea drury (Lepidoptera: Arctiidae). Invertebr. Surviv. J. 7:251-261.

Zorzetti, J., A.P.S. Ricietto, F.A.P. Fazion, A. M. Meneghin, P.M.O.J. Neves, L.A. Vilas-Boas, and G.T. Vilas-Bôas. 2018. Isolation, morphological and molecular characterization of Bacillus thuringiensis strains against Hypothenemus hampei Ferrari (Coleoptera: Curculionidae: Scolytinae). Rev. Bras. Entomol. 62:198-204. doi:10.1016/j.rbe.2018.07.002

Publicado

2020-05-01

Cómo citar

Mesén-Porras, E. A., Dahdouh-Cabia, S., Jiménez-Quirós, C., Mora-Castro, R., Rodríguez, C., & Pinto-Tomás, A. A. (2020). Inhibidores de proteasas de soya incrementan la toxicidad de Bacillus thuringiensis subs. israelensis contra Hypothenemus hampei. Agronomía Mesoamericana, 31(2), 461–478. https://doi.org/10.15517/am.v31i2.36573