Una revisión sobre biocontroladores de Phytophthora capsici y su impacto en plantas de Capsicum: Una perspectiva desde el exterior al interior de la planta

Autores

  • Edwin Quispe-Quispe Laboratory of Phytopathology, Faculty of Agronomic Engineering, Technical University of Manabí, Experimental Campus La Teodomira, km 13.5, Santa Ana, Manabí
  • Anthony A. Moreira-Morrillo Laboratory of Phytopathology, Faculty of Agronomic Engineering, Technical University of Manabí, Experimental Campus La Teodomira, km 13.5, Santa Ana, Manabí
  • Felipe Rafael Garcés-Fiallos Laboratory of Phytopathology, Faculty of Agronomic Engineering, Technical University of Manabí, Experimental Campus La Teodomira, km 13.5, Santa Ana, Manabí

DOI:

https://doi.org/10.17268/sci.agropecu.2022.025

Palavras-chave:

ají, pimiento, bioestimulantes, control biológico, inducción de resistencia

Resumo

Phytophthora capsici es un oomiceto que causa diversos síntomas como pudrición de raíz, cuello, tallo y fruto, y tizón foliar en diversas especies vegetales que incluye el género Capsicum. Una de las herramientas para contrarrestar este problema biótico, y que tal vez sea más rentable y respetuosa con el medio ambiente a largo plazo, es el uso de biocontroladores como Bacillus, Pseudomonas, Streptomyces (bacterias) y Trichoderma (hongo). Parece que cada uno de estos microorganismos poseen diferentes mecanismos que les permiten inhibir y reducir el crecimiento de P. capsici, afectando negativamente su desarrollo de esporangios, germinación y motilidad de zoosporas, y crecimiento del tubo germinativo. Aunque parecería que esta acción biocontroladora directa sobre el fitopatógeno está correlacionada con la reducción de síntomas en plantas de Capsicum u otras especies vegetales, que también involucraría la activación de respuestas de defensa en plantas contra P. capsici inducidas por los microorganismos. Estos pueden estimular en plantas infectadas o no con P. capsici, la actividad de varias enzimas relacionadas a las vías de isoflavonoides y especies reactivas de oxígeno, así como la expresión de diferentes genes que codifican proteínas relacionadas con la patogénesis, y otras proteínas que pueden activar las vías de señalización del ácido jasmónico, ácido salicílico o etileno. A pesar de los pocos trabajos existentes relacionados con la interacción bioquímica y molecular de CapsicumP. capsici–biocontrolador, en esta revisión se ha esquematizado y elucidado los posibles efectos y rutas metabólicas relacionadas a ese sistema vegetal tripartito.

Referências

Abbasi, S., Spor, A., & Sadeghi, A. (2021). Streptomyces strains modulate dynamics of soil bacterial communities and their efficacy in disease suppression caused by Phytophthora capsici. Scientific Reports, 11, 9317.

Abeysekara, N. S., Hickman, H., Westhafer, S., Johnson, G. C., Evans, T. A., Gregory, N. F., & Donofrio, N. M. (2019). Characterization of Phytophthora capsici isolates from lima bean grown in Delaware, United States of America. PhytopathologiaMediterranea, 58, 535-546.

Ahmed, A. S., Perez-Sanchez, C., Egea, C., Candela, M. E. (1999). Evaluation of Trichoderma harzianum for controlling root rot caused by Phytophthora capsici in pepper plants. Plant Pathology, 48(1), 58-65.

Amaresan, N., Kumar, K., Naik, J. H., Bapatla, K. G., & Mishra, R. K. (2018). Streptomyces in Plant Growth Promotion: Mechanisms and Role. In B. P. Singh, V. K. Gupta, & A. K. Passari (Eds.). New and Future Developments in Microbial Biotechnology and Bioengineering, Chapter 8: 125–135.

Amrani, S., & Abdel-Azeem, A. M. (2018). Checklist of Algerian fungi–Part 2: Chromistan fungal analogues (Oomycota, Bigyra, Cercozoa). Microbial Biosystems, 3(2), 13-28.

Andrić, S., Meyer, T., & Ongena, M. (2020). Bacillus responses to plant-associated fungal and bacterial communities. Frontiers in Microbiology, 11, 1350.

Bae, H., Roberts, D. P., Lim, H. S., Strem, M. D., Park, S. C., et al. (2011). Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Molecular Plant-microbe Interactions, 24(3), 336–351.

Baysal, O., Turgut, C., & Mao, G. (2005). AcibenzolarSmethyl induced resistance to Phytophthora capsici in pepper leaves. Plant Biology, 49(1), 599-604.

Barboza, E. A., Fonseca, M. E. N., Boiteux, L. S., & Reis, A. (2017). First worldwide report of a strawberry fruit rot disease caused by Phytophthora capsici isolates. Plant Disease, 101, 259-259.

Bhusal, B., &Mmbaga, M. T. (2020). Biological control of Phytophthora blight and growth promotion in sweet pepper by Bacillus species. Biological Control, 150, 104373.

Bissett, J., Gams, W., Jaklitsch, W., & Samuels, G. J. (2015). Accepted Trichoderma names in the year 2015. IMA fungus, 6(2), 263-295.

Brakhage, A. A. (2013). Regulation of fungal secondary metabolism. Nature Reviews Microbiology, 11(1), 21-32.

Cerkauskas, R. F., Ferguson, G., & MacNair, C. (2015). Management of Phytophthora blight (Phytophthora capsici) on vegetables in Ontario: Some greenhouse and field aspects. Canadian Journal of Plant Pathology, 37(3), 285-304.

Chemeltorit, P. P., Mutaqin, K. H., & Widodo, W. (2017). Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10–86: a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. European Journal of Plant Pathology, 147, 157-166.

Chen, Y., Chen, P., & Tsay, T. T. (2016). The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsici. Biological Control, 98, 34-42.

Diánez, F., Santos, M., Carretero Marín, F. (2015). Trichoderma saturnisporum, a new biological control agent. Science of Food and Agriculture, 96, 1934-1944.

Dimkić, I., Janakiev, T., Petrović, M., Degrassi, G., Fira, D. (2022). Plant-associated Bacillus and Pseudomonas antimicrobial activities in plant disease suppression via biological control mechanisms - A review. Physiological and Molecular Plant Pathology, 117(1), 101754.

Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. American Phytopathological Society (APS Press).

Esquivel-Cote, R., Gavilanes-Ruiz, M., Cruz-Ortega, R., & Huante, P. (2013). Importancia agrobiotecnológica de la enzima ACC desaminasa en rizobacterias, una revisión. Revista Fitotecnia Mexicana, 36(3), 251-258.

Ezziyyani, M., Sánchez, C. P., Requena, M. E., Rubio, L., & Castillo, M. E. (2004). Biocontrol por Streptomyces rochei –Ziyani–, de la podredumbre del pimiento (Capsicum annuum L.) causada por Phytophthora capsici. Gaceta Sanitaria, 26, 69-78.

Fickers, P. (2012). Antibiotic Compounds from Bacillus: Why are they so Amazing? American Journal of Biochemistry and Biotechnology, 8(1), 38–43.

Gaibor-Vaca, D., García-Bazurto, G., & Garcés-Fiallos, F. R. (2022). Mecanismos de defensa en plantas de Capsicum contra Phytophthora capsici. Revista Bionatura, 7(2), 25.

Garcés-Fiallos, F. R., Saltos, A., Corozo-Quiñonez, L., Pacheco-Coello, L., Santos-Ordóñez, R., & Urresta, L. F., et al. (2022). Capsicum hypocotyls mycobiome diversity is unaffected by Phytophthora capsici inoculation. Physiological and Molecular Plant Pathology, 118, 101801.

Gevens, A. J., Roberts, P. D., McGovern, R. J., & Kucharek, T. A. (2011). Vegetable diseases caused by Phytophthora capsici in Florida. Plant Pathology Department SP159. Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida.

Gilardi, G., Vasileiadou, F., Garibaldi, A., Gullino, M. L. (2021). Biocontrol agents and resistance inducers reduce Phytophthora crown rot (Phytophthora capsici) of sweet pepper in closed soilless culture. Phytopathologia Mediterranea, 60(1), 149-163.

Granke, L. L., Quesada-Ocampo, L., Lamour, K., & Hausbeck, M. K. (2012). Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant disease, 96(11), 1588-1600.

Hadar, Y., & Papadopoulou, K. K. (2012). Suppressive composts: microbial ecology links between abiotic environments and healthy plants. Annual Review of Phytopathology, 50, 133–153.

Hashem, A., Tabassum, B., & Abd-Allah, E. F. (2019). Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences, 26(6), 1291–1297.

Hermosa, R., Rubio, M. B., Cardoza, R. E., Nicolás, C., Monte, E., Gutiérrez, S. (2023). The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology, 16(2), 69–80.

Hernández-Melchor, D. J., Ferrera-Cerrato, R., & Alarcón, A. (2019). Trichoderma: agricultural and biotechnological importance, and fermentation systems for producing biomass and enzymes of industrial interest. Chilean Journal of Agricultural & Animal Sciences, 35(1), 98-112.

Hoitink, H. A., Madden, L. V., & Dorrance, A. E. (2006). Systemic resistance induced by Trichoderma spp.: interactions between the host, the pathogen, the biocontrol agent, and soil organic matter quality. Phytopathology, 96(2), 186–189.

Huallanca, C. A., & Cadenas, C. A. (2014). Control of Phytophthora capsici Leonian in Capsicum annuum cv. king papri with fungicides, fertilizers and biocontrol agents. In Anales Científicos, 75(1), 130-137.

Hyder, S., Gondal, A. S., Rizvi, Z. F., Ahmad, R., Mohsin, M., et al. (2020). Characterization of native plant growth promoting rhizobacteria and their anti-oomycete potential against Phytophthora capsici affecting chilli pepper (Capsicum annum L.). Scientific Reports, 10, 13859.

Izzeddin, N., & Medina, L. (2011). Efecto del control biológico por antagonistas sobre fitopatógenos en vegetales de consumo humano. Salus,15(3), 8-12.

Islam, S. Z., Babadoost, M., Lambert, K. N., Ndeme, A., & Fouly, H. M. (2005). Characterization of Phytophthora capsici isolates from processing pumpkin in Illinois. Plant Disease, 89(2), 191-197.

Jayalakshmi, R., Oviya, R., Premalatha, K., Mehetre, S. T., Paramasivam, M. et al. (2021). Production, stability and degradation of Trichoderma gliotoxin in growth medium, irrigation water and agricultural soil. Scientific Reports, 11, 16536.

Jayaraman, S., Naorem, A., Lal, R., Dalal, R. C., Sinha, N. K., Patra, A. K., & Chaudhari, S. K. (2021). Disease-Suppressive Soils—Beyond food production: a critical review. Journal of Soil Science and Plant Nutrition, 21, 1437–1465.

Jiang, H., Zhang, L., Zhang, J. Z., Ojaghian, M. R., & Hyde, K. D. (2016). Antagonistic interaction between Trichoderma asperellum and Phytophthora capsici in vitro. Journal of Zhejiang University. Science B, 17(4), 271–281.

Jung, T., Nechwatal, J., Cooke, D. E. L., Hartmann, G., Blaschke, M., et al. (2003). Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycological Research, 107(7), 772-789.

Khatun, A., Farhana, T., Sabir, A. A., Islam, S., West, H. M., Rahman, M., & Islam, T. (2018). Pseudomonas and Burkholderia inhibit growth and asexual development of Phytophthora capsici. Zeitschrift für Naturforschung C, Journal of Biosciences, 73(3-4), 123–135.

Khushboo, K. P., Dubey, K. K., Usmani, Z., Sharma, M., Gupta, V. K. (2022). Biotechnological and industrial applications of Streptomyces metabolites. Biofuels Bioproducts Biorefining, 16, 244–264.

Köhl, J; Kolnaar, R; Ravensberg, W. J. (2019). Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science, 10, 845.

Küçük, Ç., & Kivanç, M. (2003). Isolation of Trichoderma spp. and determination of their antifungal, biochemical and physiological features. Turkish Journal of Biology, 27(4), 247- 253.

Lamour, K. H., Stam, R., Jupe, J., & Huitema, E. (2012). The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13, 329-337.

La Spada, F., Stracquadanio, C., Riolo, M., Pane, A., & Cacciola, S.O. (2020). Trichoderma counteracts the challenge of Phytophthora nicotianae infections on tomato by modulating plant defense mechanisms and the expression of crinkler, necrosis-inducing Phytophthora Protein 1, and cellulose-binding elicitor lectin pathogenic effectors. Frontiers in plant science, 11, 583539.

Lagunas, J., Zavaleta, E., Osada, S., Aranda, S., Luna, I., & Vaquera, H. (2001). Bacillus firmus como agente de control biológico de Phytophthora capsici Leo. en jitomate (Lycopersicon esculentum Mill.). Revista Mexicana de Fitopatología, 19(1), 57-65.

Lahlali, R., Ezrari, S., Radouane, N., Kenfaoui, J., Esmaeel, Q., et al. (2022). Biological control of plant pathogens: a global perspective. Microorganisms, 10(3), 596.

Lee, J. Y., Moon, S. S., & Hwang, B. K. (2003). Isolation and in vitro and in vivo activity against Phytophthora capsici and Colletotrichum orbiculare of phenazine-1-carboxylic acid from Pseudomonas aeruginosa strain GC-B26. Pest Management Science, 59(8), 872–882.

Lee, K. J., Kamala-Kannan, S., Sub, H. S., Seong, C. K., & Lee, G. W. (2008). Biological control of Phytophthora blight in red pepper (Capsicum annuum L.) using Bacillus subtilis. World Journal of Microbiology and Biotechnology, 24(7), 1139-1145.

Ley-López, N., Márquez-Zequera, I., Carrillo-Fasio, J.A., León-Félix, J., Cruz-Lachica, I., et al. (2018). Effect of biocontrol and germinative inhibition of Bacillus spp. on zoospores of Phytophthora capsici. Revista Mexicana de Fitopatología, 36(2), 215-232.

Ley-López, N., Basilio Heredia, J., San Martín-Hernández, C., Ibarra-Rodríguez, J. R., Angulo-Escalante, M. Á., & García-Estrada, R. S. (2022). Biosíntesis inducida de fengicina y surfactina en una cepa de Bacillus amyloliquefaciens con actividad oomiceticida sobre zoosporas de Phytophthora capsici. Revista Argentina de Microbiologia, (In press).

Li, H., Cai, X., Gong, J., Xu, T., Ding, G-c., & Li, J. (2019). Long-term organic farming manipulated rhizospheric microbiome and Bacillus antagonism against pepper blight (Phytophthora capsici). Frontiers in Microbiology, 10, 342.

Li, Y., Feng, X., Wang, X., Zheng, L., & Liu, H. (2020). Inhibitory effects of Bacillus licheniformis BL06 on Phytophthora capsici in pepper by multiple modes of action. Biological Control, 144, 104210.

Miao, J., Cai, M., Dong, X., Liu, L., Lin, D., Zhang, C., Pang, Z & Liu, X. (2016). Evaluación de la resistencia a oxatiapiprolina en Phytophthora capsici y detección de una mutación puntual (G769W) en PcORP1 que confiere resistencia. Frontiers in Microbiology, 7, 615.

Morán-Díaz, M. E., Martínez de Alba, Á. E., Rubio, M. B., Hermosa, R., & Monte, E. (2021). Trichoderma and the Plant Heritable Priming Responses. Journal of Fungi, 7(4), 318.

Moreira-Morrillo, A. A., Monteros-Altamirano, Á., Reis, A., & Garcés-Fiallos, F. R. (2022). Phytophthora capsici on Capsicum Plants: A Destructive Pathogen in Chili and Pepper Crops. In (Ed.), Capsicum - New Perspective. IntechOpen.

Mukherjee, P. K., Horwitz, B. A., Herrera-Estrella, A., Schmoll, M., & Kenerley, C. M. (2013). Trichoderma research in the genome era. Annual Review of Phytopathology, 51, 105-129.

Nguyen, X.-H., Naing, K.-W., Lee, Y.-S., Tindwa, H., Lee, G.-H., Jeong, B.-K., & Kim, K.-Y. (2012). Biocontrol potential of Streptomyces griseus H7602 against root rot disease (Phytophthora capsici) in pepper. The Plant Pathology Journal. 28(3), 282-289.

Nguyen, X. H., Naing, K. W., Lee, Y. S., Kim, Y. H., Moon, J. H., & Kim, K. Y. (2015). Antagonism of antifungal metabolites from Streptomyces griseus H7602 against Phytophthora capsici. Journal of Basic Microbiology, 55(1), 45–53.

Ortiz, E., & Camargo, L. (2005). Doenças da Nogueira Pecan. En H. Kimati, L. Amorin, A. Bergamin, L. Camargo, & J. Rezende, Manual de Fitopatologia (págs. 530-535). São Paulo: Agronômica Ceres Ltda.

Özyilmaz, U., & Benlioglu, K. (2013). Enhanced biological control of Phytophthora blight of pepper by biosurfactant-producing Pseudomonas. The Plant Pathology Journal, 29(4), 418–426.

Pal, K. K., & Gardener, B. M. (2006). Biological control of plant pathogens. The Plant Health Instructor.

Pang, Z., Shao, J., Chen, L., Lu, X., Hu, J., Qin, Z., & Liu, X. (2013). Resistance to the novel fungicide pyrimorph in Phytophthora capsici: risk assessment and detection of point mutations in CesA3 that confer resistance. PLoS One, 8(2), e56513.

Park, K., Park, Y. S., Ahamed, J., Dutta, S., Ryu, H., Lee, S H., Balaraju, K., Manir, M., & Moon, S. S. (2016). Elicitation of induced systemic resistance of chili pepper by iturin A analogs derived from Bacillus vallismortis EXTN-1. Canadian Journal of Plant Science, 96(4), 564-570.

Paul, D., & Sarma, Y. R. (2006) Antagonistic effects of metabolites of Pseudomonas fluorescens strains on the different growth phases of Phytophthora capsici, foot rot pathogen of black pepper (Piper nigrum L.), Archives of Phytopathology and Plant Protection, 39(2), 113-118.

Pedraza, L. A., López, C. E., & Uribe-Vélez, D. (2020). Mechanisms of action of Bacillus spp. (Bacillaceae) against phytopathogenic microorganisms during their interaction with plants. Acta Biológica Colombiana, 25(1), 112-125.

Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., Bakker, P. A. H. M. (2014). Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, 52, 347-375.

Poveda, J. (2021). Trichoderma as biocontrol agent against pests: New uses for a mycoparasite. Biological Control, 159, 104634.

Quesada-Ocampo, L. M., & Hausbeck, M. K. (2010). Resistance in tomato and wild relatives to crown and root rot caused by Phytophthora capsici. Phytopathology, 100(6), 619-627.

Ramírez, C., Soto, Z., Castro, L., Arauz, L. F., Uribe-Lorío, L., & Uribe, L. (2015). Efecto de cuatro rizobacterias promotoras de crecimiento sobre la pudrición basal causada por Phytophthora capsici en plantas de chile dulce (Capsicum annuum). Agronomía Costarricense, 39(Suppl. 1), 87-100.

Ramírez-Valdespino, C.A., Casas-Flores, S., & Olmedo-Monfil, V. (2019). Trichodermaas a model to study effector-like molecules. Frontiers in Microbiology, 10, 1030.

Reis, A., Paz-lima, M. L., Moita, A.W.,Aguiar, F. M., Fonseca, M. E., Café-Filho, A. C., & Boiteux, L. S.(2018). A reappraisal of the natural and experimental host range of neotropical Phytophthora capsici isolates from Solanaceae, Cucurbitaceae, Rosaceae, and Fabaceae. Journal of Plant Pathology,100, 215-223.

Ristaino, J. B., & Johnston, S. A. (1999). Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease, 83(12), 1080-1089.

Roskov, Y., Abucay, L., Orrell, T., Nicolson, D., Flann, C., et al. (2016). Species 2000 & ITIS Catalogue of Life, 2016 Annual Checklist.

Saltos, L. A., Corozo-Quiñónez, L., Pacheco-Coello, R., Santos-Ordóñez, E., Monteros-Altamirano, A., & Garcés-Fiallos, F. R. (2021). Tissue specific colonization of Phytophthora capsici in Capsicum spp.: molecular insights over plant-pathogen interaction. Phytoparasitica, 49, 113–122.

Saltos, L. A., Monteros-Altamirano, Á., Reis, A., Garcés-Fiallos, F. R. (2022). Phytophthora capsici: the diseases it causes and management strategies to produce healthier vegetable crops. Horticultura Brasileira, 40, 5-17.

Sang, M. K., Shrestha, A., Kim, D. Y., Park, K., Pak, C. H., & Kim, K. D. (2013). Biocontrol of Phytophthora blight and anthracnose in pepper by sequentially selected antagonistic rhizobacteria against Phytophthora capsici. The Plant Pathology Journal, 29(2), 154–167.

Segarra, G., Casanova, E., Bellido, D., Odena, M. A., Oliveira, E., &Trillas, I. (2007). Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics, 7(21), 3943-3952.

Segarra, G., Avilés, M., Casanova, E., Borrero, C., & Trillas, I. (2013). Effectiveness of biological control of Phytophthora capsici in pepper by Trichoderma asperellum strain T34. Phytopathologia Mediterranea, 52(1), 77–83.

Serrano-Carreon, L., Hathout, Y., Bensoussan, M., & Belin, J. M. (1993). Metabolism of linoleic acid or mevalonate and 6-pentyl-α-pyrone biosynthesis by Trichoderma species. Applied and Environmental Microbiology, 59(9), 2945-2950.

Shafi, J., Tian, H., & Ji, M. (2017). Bacillus species as versatile weapons for plant pathogens: a review. Biotechnology & Biotechnological Equipment, 31(3), 446-459.

Sharma, V., Salwan, R., & Sharma, P.N. (2017). The comparative mechanistic aspects of Trichoderma and probiotics: scope for future research. Physiological and Molecular Plant Pathology, 100, 84-96.

Shobha, M. S., Lakshmi, D. N., & Mahadeva M. S. (2019). Induction of systemic resistance by rhizobacterial and endophytic fungi against foot rot disease of Piper nigrum L. by increasing enzyme defense activity. International Journal of Environment, Agriculture and Biotechnology, 4(1), 86-98.

Sid Ahmed, A., Pérez‐Sánchez, C., Egea, C., & Candela, M. E. (1999). Evaluation of Trichoderm aharzianum for controlling root rot caused by Phytophthora capsici in pepper plants. Plant Pathology, 48(1), 58-65.

Syed-Ab-Rahman, S. F., Xiao, Y., Carvalhais, L. C., Ferguson, B. J., Schenk, P. M. (2019). Suppression of Phytophthora capsici infection and promotion of tomato growth by soil bacteria. Rhizosphere, 9, 72-75.

Syed-Ab-Rahman, S. F., Chua, E. T., & Schenk, P. M. (2021). Characterisation and isolation of bioactive compounds of anti-oomycete bacterial isolates inhibiting the growth of Phytophthora capsici. Australasian Plant Pathology, 50, 651–659.

Tančić-Živanov, S., Medić-Pap, S., Danojević, D., & Prvulović, D. (2020). Effect of Trichoderma spp. on growth promotion and antioxidative activity of pepper seedlings. Brazilian Archives of Biology and Technology, 63, e20180659.

Thankappan, S., Narayanasamy, S., Sridharan, A. P., Binodh, A. K ., Nirmala A., Parasuraman, P., & Uthandi, S. (2022). Rhizospheric volatilome in modulating induced systemic resistance against biotic stress: A new paradigm for future food security. Physiological and Molecular Plant Pathology, 120,101852.

Tomah, A. A., Alamer, I. S., Li, B., & Zhang, J. Z. (2020). A new species of Trichoderma and gliotoxin role: A new observation in enhancing biocontrol potential of T. virens against Phytophthora capsici on chili pepper. Biological Control, 145, 104261.

Trinidad-Cruz, J. R., Rincón-Enríquez, G., Evangelista-Martínez, Z., & Quiñones-Aguilar, E. E. (2021). Biorational control of Phytophthora capsici in pepper plants using Streptomyces spp. Revista Chapingo. Serie horticultura, 27(2), 85-99.

Tyśkiewicz, R., Nowak, A., Ozimek, E., & Jaroszuk-Ściseł, J. (2022). Trichoderma: the current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. International Journal of Molecular Sciences, 23(4), 2329.

Umadevi, P., Anandaraj, M. (2019). Proteomic analysis of the tripartite interaction between black pepper, Trichoderma harzianum and Phytophthora capsici provides insights into induced systemic resistance mediated by Trichoderma spp. European Journal of Plant Pathology, 154, 607–620.

Wang, Z., Ni, X., Peng, Q., Hou, Y., Fang, Y., et al. (2018). The novel fungicide SYP-14288 acts as an uncoupler against Phytophthora capsici. Pesticide Biochemistry and Physiology, 147, 83-89.

Yedidia, I., Benhamou, N., Kapulnik, Y., & Chet, I. (2000). Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiology and Biochemistry, 38(11), 863-873.

Zhang, S., Gan, Y., & Xu, B. (2016). Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Frontiers in Plant Science, 7, 1405.

Zohara, F., Akanda, M. A. M., Paul, N. C., Rahman, M., & Islam, M. T. (2016). Inhibitory effects of Pseudomonas spp. on plant pathogen Phytophthora capsici in vitro and in planta. Biocatalysis and Agricultural Biotechnology, 5, 69-77.

Publicado

2022-09-21

Como Citar

Quispe-Quispe, E. ., Moreira-Morrillo, A. A. ., & Garcés-Fiallos, F. R. (2022). Una revisión sobre biocontroladores de Phytophthora capsici y su impacto en plantas de Capsicum: Una perspectiva desde el exterior al interior de la planta. Scientia Agropecuaria, 13(3), 275-289. https://doi.org/10.17268/sci.agropecu.2022.025

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Artículos de Revisión