Efficacy of Aqueous Plant Extracts in the Control of Downy Mildew (Peronospora variabilis) in Quinoa (Chenopodium quinoa)

Rolando Bautista-Gómez, Walter Mateu-Mateo, Miquer Aybar-Cordero, Victor Chávez-Centeno, Francisco Alejandro Espinoza-Montes

Abstract

Downy mildew caused by Peronospora variabilis is one of the main health problems affecting quinoa cultivation in the Andean region. The objective of this study was to evaluate the efficacy of aqueous extracts of garlic (Allium sativum), horsetail (Equisetum bogotense), and paico (Chenopodium ambrosioides) in reducing the severity of downy mildew and its effect on the yield of the Blanca Junín and Pasankalla quinoa varieties. The working solutions contained 10% of the crude extract. Foliar applications were made every 7 days, between 21 and 84 days after sowing. Using a randomized complete block split-plot design, severity, area under the disease progress curve (AUDPC), and relative efficacy (RE) of the treatment were quantified. The results revealed a significant interaction between variety and treatment (p < 0.05). Garlic extract in the Blanca Junín variety stood out as the best alternative for downy mildew control, considerably reducing AUDPC, increasing yield, and demonstrating greater RE (68.4%) compared to the synthetic fungicide metalaxyl. In the Pasankalla variety, because of its greater intrinsic tolerance, the impact of the extracts on yield was less pronounced. These findings position plant extracts, especially garlic extracts, as viable alternatives for the integrated management of downy mildew in quinoa crops, although it is recommended to validate their effectiveness in multiple campaigns that align with environmental sustainability and human health.

Keywords

botanical extracts; effective biofungicides; genotypic response; oomycete control; organosulfur compounds

Full Text:

PDF

References

Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18(2), 265–267. https://doi.org/10.1093/jee/18.2.265a

Apaza Ticona, J., Alanoca Arocutipa, V., Cutipa Añamuro, G., Calderon Torres, A., Quenta Paniagua, R. A., & Apaza Chino, G. (2022). Sabiduría tradicional para la crianza de cultivo de quinua (Chenopodium quinoa Willd.) y uso en las comunidades aymaras (Puno-Perú). Anales de Geografía de la Universidad Complutense, 42(1), 11–30. https://doi.org/10.5209/aguc.81793

Bazile, D. (2024). Perspectivas de granos andinos en Europa y en el mundo: la quinoa, desafíos y perspectivas de una conquista del mundo. Día Nacional de los Granos Andinos (pp. 3-p). Centro de Investigación e Innovación en Productos Derivados de Cultivos Andinos. Retrieved from https://hal.science/hal-05182285/document

Bazile, D., Bertero, D., & Nieto, C. (2015). State of the art report of quinoa around the world in 2013. FAO & CIRAD. Retrieved from https://openknowledge.fao.org/handle/20.500.14283/i4042e

Cenobio-Galindo, A. D. J., Hernández-Fuentes, A. D., González-Lemus, U., Zaldívar-Ortega, A. K., González-Montiel, L., Madariaga-Navarrete, A., & Hernández-Soto, I. (2024). Biofungicides based on plant extracts: On the road to organic farming. International Journal of Molecular Sciences, 25(13), 6879. https://doi.org/10.3390/ijms25136879

Christensen, S. A., Pratt, D. B., Pratt, C., Nelson, P. T., Stevens, M. R., Jellen, E. N., & Maughan, P. J. (2007). Assessment of genetic diversity in the USDA and CIP-FAO international nursery collections of quinoa (Chenopodium quinoa Willd.) using microsatellite markers. Plant Genetic Resources, 5(2), 82–95. https://doi.org/10.1017/S1479262107672293

Colque-Little, C., Abondano, M. C., Lund, O. S., Amby, D. B., Piepho, H. P., Andreasen, C., ... & Schmid, K. (2021). Genetic variation for tolerance to the downy mildew pathogen Peronospora variabilis in genetic resources of quinoa (Chenopodium quinoa Willd.). BMC Plant Biology, 21(1), 41. https://doi.org/10.1186/s12870-020-02804-7

Cruces, L., Callohuari, Y., & Carrera, C. (2016). Quinua, manejo integrado de plaga. Estrategias en el cultivo de la quinua para fortalecer el sistema agroalimentario en la zona andina. Organización de las Naciones Unidas para la Alimentación y la Agricultura (FAO). Retrieved from http://www.fao.org/3/a-i6038s.pdf

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

Dalal, A., Attia, Z., & Moshelion, M. (2017). To produce or to survive: How plastic is your crop stress physiology? Frontiers in Plant Science, 8, 2067. https://doi.org/10.3389/fpls.2017.02067

Danielsen, S., & Ames, T. (2008). El mildiu (Peronospora farinosa) de la quinua (Chenopodium quinoa Willd.) en la zona andina: Manual práctico para el estudio de la enfermedad y del patógeno. Centro Internacional de la Papa (CIP). Retrieved from https://cipotato.org/wp-content/uploads/2014/10/AN60198.pdf

Danielsen, S., & Munk, L. (2004). Evaluation of disease assessment methods in quinoa for their ability to predict yield loss caused by downy mildew. Crop Protection, 23(3), 219–228. https://doi.org/10.1016/j.cropro.2003.08.010

Danielsen, S., Bonifacio, A., & Ames, T. (2003). Diseases of quinoa (Chenopodium quinoa Willd.). Food Reviews International, 19(1–2), 43–59. https://doi.org/10.1081/FRI-120018867

Danielsen, S., Jacobsen, S. E., & Hockenhull, J. (2002). First report of downy mildew of quinoa caused by Peronospora farinosa f. sp. Chenopodii in Denmark. Plant Disease, 86(10), 1175. https://doi.org/10.1094/PDIS.2002.86.10.1175B

Estrada-Zúniga, R., Apaza-Mamani, V., Pérez-Ávila, A. A., Altamirano-Pérez, A. M., Neyra-Valdez, E., & Bobadilla, L. G. (2022). Comportamiento agronómico de 81 genotipos de quinua (Chenopodium quinoa Willd.) en el Perú. Ecosistemas y recursos agropecuarios, 9(1), 3134. https://doi.org/10.19136/era.a9n1.3134

Fufa, B. K. (2019). Anti-bacterial and anti-fungal properties of garlic extract (Allium sativum): A review. Microbiology Research Journal International, 28(3), 1–5. https://doi.org/10.9734/mrji/2019/v28i330133

Fukuzaki, S. (2006). Mechanisms of actions of sodium hypochlorite in cleaning and disinfection processes. Biocontrol Science, 11(4), 147–157. https://doi.org/10.4265/bio.11.147

Galecio-Julca, M., Neira-Ojeda, M., Chanduvi-García, R., Peña-Castillo, R., Álvarez-Bernaola, L. A., Granda-Wong, C., ... & Morales-Pizarro, A. (2023). Efecto de la eficacia de los microorganismos nativos y la composta en tres pisos altitudinales en el cultivo de quinua (Chenopodium quinoa) variedad INIA 415-Pasankalla. Terra Latinoamericana, 41, 1–12. https://doi.org/10.28940/terra.v41i0.1622

García, D., Ramos, A. J., Sanchis, V., & Marín, S. (2013). Equisetum arvense hydro‐alcoholic extract: Phenolic composition and antifungal and antimycotoxigenic effect against Aspergillus flavus and Fusarium verticillioides in stored maize. Journal of the Science of Food and Agriculture, 93(9), 2248–2253. https://doi.org/10.1002/jsfa.6033

García-Torres, S. M., Teixeira, J. A., Encina-Zelada, C. R., Silva, C. L., & Gomes, A. M. (2025). Effect of different disinfection procedures on the microbiological quality and germination efficacy of sprouted quinoa (Chenopodium quinoa Willd.) flour. Foods, 14(18), 3196. https://doi.org/10.3390/foods14183196

Gisi, U., & Cohen, Y. (1996). Resistance to phenylamide fungicides: A case study with Phytophthora infestans involving mating type and race structure. Annual Review of Phytopathology, 34(1), 549–572. https://doi.org/10.1146/annurev.phyto.34.1.549

Hanson, K., & Shattock, R. C. (1998). Effect of metalaxyl on formation and germination of oospores of Phytophthora infestans. Plant Pathology, 47(2), 116–122. https://doi.org/10.1046/j.1365-3059.1998.00215.x

Hayat, S., Cheng, Z., Ahmad, H., Ali, M., Chen, X., & Wang, M. (2016). Garlic, from remedy to stimulant: Evaluation of antifungal potential reveals diversity in phytoalexin allicin content among garlic cultivars; allicin containing aqueous garlic extracts trigger antioxidants in cucumber. Frontiers in Plant Science, 7, 1235. https://doi.org/10.3389/fpls.2016.01235

Jaramillo, B. E., Duarte, E., & Delgado, W. (2012). Bioactividad del aceite esencial de Chenopodium ambrosioides colombiano. Revista Cubana de Plantas Medicinales, 17(1), 54–64. Retrieved from https://www.medigraphic.com/pdfs/revcubplamed/cpm-2012/cpm121f.pdf

Kumar, R., Mishra, A. K., Dubey, N. K., & Tripathi, Y. B. (2007). Evaluation of Chenopodium ambrosioides oil as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. International Journal of Food Microbiology, 115(2), 159–164. https://doi.org/10.1016/j.ijfoodmicro.2006.10.017

Langsi, D. J., Nukenine, E. N., Fokunang, C. N., Suh, C., & Goudoungou, W. J. (2017). Potentials of essential oils of Chenopodium ambrosioides L. and Cupressus sempervirens L. against stored maize pest, Sitophilus zeamais Motschulsky. Journal of Entomology and Zoology Studies, 5(2), 309–313. Retrieved from https://www.entomoljournal.com/archives/2017/vol5issue2/PartE/5-1-238-716.pdf

Li, S., & Zhihui, C. (2008). Allium sativum extract as a biopesticide affecting pepper blight. International Journal of Vegetable Science, 15(1), 13–23. https://doi.org/10.1080/19315260802446377

Makia, R., Al.sammarrae, K. W., Al-Halbosiy, M. M., & Al-Mashhadani, M. H. (2022). Phytochemistry of the genus Equisetum (Equisetum arvense). GSC Biological and Pharmaceutical Sciences, 18(02), 283–289. https://doi.org/10.30574/gscbps.2022.18.2.0059

Norman, D. W., Worman, F. D., Siebert, J. D., & Modiakgotla, E. (1995). The farming systems approach to development and appropriate technology generation. Rome: FAO Publication. Retrieved from https://www.fao.org/4/v5330e/v5330e00.htm

Pando, L., & Aguilar, E. (2016). Guía de cultivo de la quinua. Organización de las Naciones Unidas para la Alimentación y la Agricultura, Universidad Nacional Agraria La Molina, 2, 17–18. Retrieved from https://openknowledge.fao.org/server/api/core/bitstreams/76594aca-c6a8-45e0-97db-39905cd72575/content/

Pánek, M., Ali, A., & Helmer, Š. (2022). Use of metalaxyl against some soil plant pathogens of the class peronosporomycetes-A review and two case studies. Plant Protection Science, 58(2), 92–109. https://doi.org/10.17221/42/2021-PPS

Pardo, M. S., Allende Burga, R., & Romero Carrión, V. L. (2020). Estudio comparativo en rendimiento y calidad de 12 variedades de quinua orgánica en la comunidad campesina de San Antonio de Manallasac, Ayacucho. Revista Campus de la Facultad de Ingeniería y Arquitectura de la Universidad de San Martin de Porres, 29, 57–66. https://doi.org/10.24265/campus.2020.v25n29.04

Pathan, S., & Siddiqui, R. A. (2022). Nutritional composition and bioactive components in quinoa (Chenopodium quinoa Willd.) greens: A review. Nutrients, 14(3), 558. https://doi.org/10.3390/nu14030558

Pérez, Á. A. (2005). Manejo del cultivo de quinua en la sierra central. Serie Manual; Nº 1-05. Instituto Nacional de Investigación y Extensión Agraria-INIA. Retrieved from https://repositorio.inia.gob.pe/server/api/core/bitstreams/0064586d-101a-4568-8d68-65093c27eff9/content

Roy, C. K., Akter, N., Sarkar, M. K., Pk, M. U., Begum, N., Zenat, E. A., & Jahan, M. A. (2019). Control of early blight of tomato caused by Alternaria solani and screening of tomato varieties against the pathogen. The Open Microbiology Journal, 13(1), 41–50. https://doi.org/10.2174/1874285801913010041

Rubén, D., Burin, D., Pereyra, E., & Heras, A. I. (2015). Quinua, regalo ancestral: Historia, contexto, tecnología, políticas. Fundación Nueva Gestión. Retrieved from https://n2t.net/ark:/13683/poQx/DzD

Ruiz, K. B., Biondi, S., Oses, R., Acuña-Rodríguez, I. S., Antognoni, F., Martinez-Mosqueira, E. A., ... & Molina-Montenegro, M. A. (2014). Quinoa biodiversity and sustainability for food security under climate change. A review. Agronomy for Sustainable Development, 34(2), 349–359. https://doi.org/10.1007/s13593-013-0195-0

Sandhu, N. S., Kaur, S. A., & Chopra, D. I. (2010). Equisetum arvense: Pharmacology and phytochemistry-a review. Asian Journal of Pharmaceutical and Clinical Research, 3(3), 146–150. Retrieved from https://web.archive.org/web/20180410062011id_/http://www.ajpcr.com/Vol3Issue3/3.pdf

Sanjai, C., Gaonkar, S. L., & Hakkimane, S. S. (2024). Harnessing nature’s toolbox: Naturally derived bioactive compounds in nanotechnology enhanced formulations. ACS Omega, 9(43), 43302–43318. https://doi.org/10.1021/acsomega.4c07756

Sarfraz, M., Nasim, M. J., Jacob, C., & Gruhlke, M. C. (2020). Efficacy of allicin against plant pathogenic fungi and unveiling the underlying mode of action employing yeast based chemogenetic profiling approach. Applied Sciences, 10(7), 2563. https://doi.org/10.3390/app10072563

Shah, H. (2014). Antibacterial and antifungal activities of the crude extracts from the stem of Chenopodium ambrosioides Linn., an indiginous medicinal plant. African Journal of Pharmacy and Pharmacology, 8(8), 231–234. https://doi.org/10.5897/AJPP2014.4010

Simko, I., & Piepho, H. P. (2012). The area under the disease progress stairs: Calculation, advantage, and application. Phytopathology, 102(4), 381–389. https://doi.org/10.1094/PHYTO-07-11-0216

Singh, J. (2008). Maceration, percolation and infusion techniques for the extraction of medicinal and aromatic plants. Extraction technologies for medicinal and aromatic plants, 67, 32–35. United Nations Industrial Development Organization, UNIDO. Retrieved from https://www.unido.org/sites/default/files/2009-10/Extraction_technologies_for_medicinal_and_aromatic_plants_0.pdf

Slusarenko, A. J., Patel, A., & Portz, D. (2008). Control of plant diseases by natural products: Allicin from garlic as a case study. Sustainable disease management in a European context. Springer. https://doi.org/10.1007/978-1-4020-8780-6_10

Sud, U. C., Ahmad, T., Gupta, V. K., Chandra, H., Sahoo, P. M., Aditya, K., ... & Biswas, A. (2017). Methodology for estimation of crop area and crop yield under mixed and continuous cropping. ICAR-Indian Agricultural Statistics Research Institute: New Delhi, India. Retrieved from https://openknowledge.fao.org/server/api/core/bitstreams/ca36b8c1-99b6-4cad-ad88-ff018647a474/content

Sureshkumar, J., Jenipher, C., Sriramavaratharajan, V., Gurav, S. S., Gandhi, G. R., Ravichandran, K., & Ayyanar, M. (2023). Genus Equisetum L: Taxonomy, toxicology, phytochemistry and pharmacology. Journal of Ethnopharmacology, 314, 116630. https://doi.org/10.1016/j.jep.2023.116630

Testen, A. L., del Mar Jiménez-Gasco, M., Ochoa, J. B., & Backman, P. A. (2014). Molecular detection of Peronospora variabilis in quinoa seed and phylogeny of the quinoa downy mildew pathogen in South America and the United States. Phytopathology, 104(4), 379–386. https://doi.org/10.1094/PHYTO-07-13-0198-R

Trebbi, G., Negri, L., Bosi, S., Dinelli, G., Cozzo, R., & Marotti, I. (2021). Evaluation of Equisetum arvense (horsetail macerate) as a copper substitute for pathogen management in field-grown organic tomato and durum wheat cultivations. Agriculture, 11(1), 5. https://doi.org/10.3390/agriculture11010005

Vega-Gálvez, A., Miranda, M., Vergara, J., Uribe, E., Puente, L., & Martínez, E. A. (2010). Nutrition facts and functional potential of quinoa (Chenopodium quinoa Willd.), an ancient Andean grain: A review. Journal of the Science of Food and Agriculture, 90(15), 2541–2547. https://doi.org/10.1002/jsfa.4158

Wang, M., Gao, L., Dong, S., Sun, Y., Shen, Q., & Guo, S. (2017). Role of silicon on plant–pathogen interactions. Frontiers in Plant Science, 8, 701. https://doi.org/10.3389/fpls.2017.00701

Wei, W., Chen, P., Khan, B., Tian, K., Feng, Y., Lv, B., ... & Liu, G. (2024). Evaluation of equisetin as an anti-microbial and herbicidal agent from endophytic fungus Fusarium sp. JDJR1. Agronomy, 14(1), 31. https://doi.org/10.3390/agronomy14010031

Refbacks

  • There are currently no refbacks.