Effect of microbial inoculants on bioactive compounds and antioxidant activity of xcat´ ik pepper (Capsicum annuum L.)
DOI:
https://doi.org/10.18633/biotecnia.v24i3.1691Keywords:
antioxidant activity, carotenoids, Capsicum annuum, microbial inoculants, sustainable agricultureAbstract
Xcat'ik pepper (Capsicum annuum L.), native to the Yucatan Peninsula, has unique organoleptic properties. However, the nutraceutical quality of the fruit has been scarcely explored and only a few previous studies have focused on improving the productive yield of the plant, hence the importance of generating knowledge in this field. The Capsicum species is considered an important food due to the content of bioactive compounds, which promote beneficial health effects. The use of microbial inoculants is an alternative to increase yield, improve fruit quality, and reduce the use of chemical fertilizers. In this work, the effect of a microbial consortium, as well as Bacillus subtilis and Trichoderma harzanium on the contents of ascorbic acid, total phenols, flavonoids, chlorophylls, carotenoids, antioxidant capacity and capsaicinoids in the fruit of xcat'ik pepper was evaluated. The obtained results were compared with an uninoculated control. Inoculations with T. harzanium and B. subtilis increased carotenoid content as well as antioxidant activity by ABTS+, in contrast the microbial consortium increased antioxidant activity by DPPH•. According to our results, the evaluated inoculants could replace chemical fertilizers, because they equal or improve the nutraceutical quality of the x'catik pepper fruit, with the advantage of being less harmful to the environment.
Downloads
References
Arimboor, R., Natarajan, R.B., Ramakrishna-Menon, K., Chandrasekar, L.K., Moorkoth, V. 2014. Red pepper (Capsicum annuum) carotenoids as a source of natural food colors: analysis and stability- a review. J Food Sci. Tecnol. 52: 1258-1271.
Baslam, M., Garmendia, I., Goicoechea N. 2011. Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. J. Agric. Food Chem. 59: 5504–5515.
Calvo, P., Nelson, L., Kloepper, J.W. 2014. Agricultural uses of plant bio stimulants. Plant Soil. 383: 3–41.
Chandrasekaran, M., Chun, S.C., Oh J.W., Paramasivan M., Saini, R.K., Sahayarayan, J.J. 2019. Bacillus subtilis CBR05 for tomato (Solanum lycopersicum) fruits in South Korea as a Novel Plant Probiotic Bacterium (PPB): implications from total phenolics, flavonoids, and carotenoids content for fruit quality. Agronomy. 9: 1–11.
Chang, C.C., Yang, M.H., Wen, H.M., Chern, J.C. 2002. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal. 10: 178–182.
Chatterjee, R., Koner, S., Datta, S. 2019. Impact of Microbial Inoculants on the Performance of Bell Pepper (Capsicum annuum L.) Varieties under Foot Hills of Eastern Himalayan Region. Int. J Curr. Microbiol. Appl. 5: 131–138.
Cisneros-Pineda, O., Torres-Tapia, L.W., Gutiérrez-Pacheco, L.C., Contreras-Martín, F., Gonzáles-Estrada, T., Peraza-Sánchez, S. 2007. Capsaicinoids cuantification in pepper peppers cultivated in the state of Yucatán México. Food Chem. 104: 1755-1760.
Cisternas-Jamet, J.R. Salvatierra-Martínez., A. Vega-Gálvez., A. Stolld., Uribe, E., Goñih, M.G. 2020. Biochemical composition as a function of fruit maturity stage of bell pepper (Capsicum annuum) inoculated with Bacillus amyloliquefaciens. Sci. Hortic-Amsterdam, 263: 1–9.
Collins, D.M., Wasmund, M.L.M., Osland, P.W.B. 1995. Improved method for quantifying capsaicinoids in Capsicum using high performance liquid chromatography. Hortscience, 30: 137–139.
Coppeta, A., Bardi, L., Bertolone, E., Berta, G. 2014. Fruit production and quality of tomato plants (Solanum lycopersicum L.) are affected by green compost and arbuscular mycorrhizal fungi. Plant Byosist, 1: 106–115.
Cruz, A.F. 2016. Effect of light-emitting diodes on arbuscular mycorrhizal fungi associated with bahiagrass (Paspalum notatum Flügge) and millet [Pennisetum glaucum (L.) R. Br]. Bioagro, 28: 163–170.
Debnath, S., Rawat, D., Kumar-Mukherjee, A., Adhikary, S., Kundu, R. 2019. Applications and Constraints of Plant Beneficial Microorganism in Agriculture. Mahyar-Mirmajlessi S., Radhakrishnan R (eds.) Biostimulants in Plants Science. IntechOpen, p. 2–25.
Dürüst, N., Dogan, S., Dürüst, Y. 1997. Ascorbic acid and element contents of food of Trabzon (Turkey). J Agric. Food Chem. 45: 2085–2087.
Esitken, A., Yildiz, H.E., Ercisli, S., Donmez, M.F., Turan, M., Gunes, A. 2010. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic-Amsterdam, 124: 62–66.
Gurung, T., Techawongstein, S., Suriharn, B., Techawongstein, S. 2011. Impact of Environments of the Accumulation of Capsaicinoids in Capsicum spp. Hortscience. 46: 1576–1581.
Hörtensteiner, S., B. Kräutler. 2011. Chlorophyll breakdown in higher plants. Biochimica et Biophysica Acta (BBA). Bioenergetics. 1807: 977–988.
Jiménez-Gómez, A., García-Estévez, I., García-Fraile, P., Escribano-Bailón, M.T., Rivas, R. 2020. Increase in phenolic compounds of Coriandrum sativum L. after the application of a Bacillus halotolerans biofertilizer. J Sci. Food Agric. 100: 2742-2749.
Karppinen, K., Zoratti, L., Nguyenquynh, N., Häggman, H., Jaakola, L. 2016. On the Developmental and Environmental Regulation of Secondary Metabolism in Vaccinium spp. Berries. 7: 1–9.
Khalid, M., Hassani, D., Bilal, M., Asad, F., Huang, D. 2017. Influence of bio-fertilizer containing beneficial fungi and rhizospheric bacteria on health promoting compounds and antioxidant activity of Spinacia oleracea L. Botanical Studies, 58: 1–9.
Kim, H.J., Chen F., Wu, C., Wang, X., Chung, H.Y., Jin, Z. 2004. Evaluation of antioxidant activity of Australian tea tree (Melaleuca alternifolia) oil and its components. Journal of Agricultural and Food Chemistry. 52: 2849–2854.
Lee, K.J., Oh, Y.C., Cho, W.K., Ma, J.Y. 2015. Antioxidant and anti-inflammatory activity determination of one hundred kinds of pure chemical compounds using offline and online screening HPLC assay. Evidence Based Complementary and Alternative Medicine, 2015: 1–13.
Li, J., Zhu, Z., Gerendás, J. 2014. Effects of nitrogen and sulfur on Total phenolics and antioxidant activity in two genotypes of leaf mustard. Journal of Plant Nutrition, 31: 1642–1655.
Lombardi, N., Caira, S., Troise, A.D., Scaloni, A., Vitaglione, P., Vinale, F., Marra, R., Salzano, A.M., Lorito, M., Woo, S.L. 2020. Thrichoderma Applications on Strawberry Plants Modulate the Physiological Processes Positively Affecting Fruit Production and Quality. Front. Microbiol. 11: 1–17.
Mellidou, I., Kanellis, A. 2017. Genetic Control of Ascorbic Acid Biosynthesis and Recycling in Horticultural Crops. Front. Chem. 5: 1–8.
Mena-Violante, H.G., Ocampo-Jiménez, O., Dendooven, L., Martínez-Soto, G., González-Castañeda, J., Davies, Jr. F.T., Olalde-Portugal, V. 2006. Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorriza. 16: 261–267.
Ógata-Gutiérrez, K., Zúñiga-Dávila, D. 2020. Bacteria-Plant interactions: an added value of microbial inoculation. Rev. Peru Biol. 27: 21–25.
Ortega-García, J.G., Montes-Belmont, R., Rodríguez-Monroy, M., Ramírez-Trujillo, J.A., Suárez-Rodríguez, R., Sepúlveda-Jiménez, G. 2015. Effect of Trichoderma asperellum applications and mineral fertilization on growth promotion and the content of phenolic compounds and flavonoids in onions. Sci. Hortic-Amsterdam, 195: 8–16.
Panche, A.N., Diwan, A.E., Chandra, S.R. 2016. Flavonoids: an overview. J Nut. Sci. 5: 1–15.
Park, Y.J., Park, S.Y., Valan-Arasu, M., Al-Dhabi N.A., Ahn, H.G., Kim, J.K., SU Park. 2017. Accumulation of carotenoids and metabolic profiling in different cultivars of tagetes flowers. Molecules, 22: 1–14.
Pascale, A., Vinale, F., Manganiello, G., Nigro, M., Lanzuise, S., Ruocco, M., Marra, R., Lombardi, N., Woo, S.L., Lorito, M. 2017. Trichoderma and its secondary metabolites improve yield and quality of grapes. J Crop Prot. 92: 176–181.
Pylac, M., Oszust, K., Frąc, M. 2019. Review report on the role of bioproducts, biopreparations, biostimulants and microbial inoculants in organic production of fruit. Rev environ. Sci. BioTech. 18: 597–616.
Ramos-Solano, B., García-Villaraco, A., Gutiérrez-Mañero, F.J., Lucas, J.A., Bonilla, A. 2013. Annual changes in bioactive contents and production in field-grown blackberry after inoculation with Pseudomonas fluorescens. Plant Physiol. Biochem. 74: 1-8.
Re, R., Pellegrini, N., Proteggiente, A., Pannala, A., Yang, M., Rice-Evans, C. 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26: 1231–1237.
Rodrigues, C.A., Nicácio, A.E., Jardim, I.C.S.F., Visentainer, J.V., & Maldaner, L. 2019. Determination of Phenolic Compounds in Red Sweet Pepper (Capsicum annuum L.) Using a Modified QuEChERS Method and UHPLC-MS/MS Analysis and Its Relation to Antioxidant Activity. J Braz Chem. Soc. 30: 1229–1240.
Rouphael, Y., Collab, G., Grazianic, G., Ritienic, A., Cardarellid, M.A. 2017. Phenolic composition, antioxidant activity and mineral profile in two seed-propagated artichoke cultivars as affected by microbial inoculants and planting time. Food Chem. 234: 10–19.
Russo, V.M., Perkins, V.P. 2010. Yield and nutrient content of bell pepper pods from plants developed from seedlings inoculated, or not, with microorganisms. Hort. Sci. 45: 352–358.
Salveit, M.E. 2017. Synthesis and Metabolism of Phenolic Compounds. Chapter 5. Fruit and Vegetable Phytochemicals: Chemistry and Human Health, 2nd Edition, Edit. Elhadi M Yahia.
Shumskaya, M., Wurtzel, E.T. 2013. The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci. 208: 58–63
Silva, L.R., Azevedo, J., Pereira, M.J., Carro, L., Velázquez, E., Peix, A., Valentao, P., Andrade, P.B. 2014. Inoculation of the nonlegume Capsicum annuum (L.) with Rhizobium strains. 1. Effect on bioactive compounds, antioxidant activity, and fruit ripeness. J. Agric. Food Chem. 62: 557–564.
Singh, D.P., Singh, V., Gupta, V.K., Shukla, R., Prabha, R., Sarma., BK., Patel, J.S. 2020. Microbial Inoculation in Rice Regulates Antioxidative Reactions and Defense Related Genes to Mitigate Drought Stress. 10: 1–17.
Singleton, V.L., Rossi, J.A Jr. 1965. Colorimetric of total phenolic with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic. 16: 144-158.
Soltani, A., Weraduwage, S.M., Sharkey, T., Lowry, D. 2019. Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relations ships. BMC Genomics, 20: 1–18.
Sood, M., Kapoor, D., Kumar, V., Sheteiwy, M.S., Ramakrishan, M., Landi, M., Franiti, A., Sharma, A. 2020. Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent. Plants. 9: 2–25.
Tag, H.M., Kelany, O.E., Tantawy, H.M., Fahmy, A.A. 2014. Potential anti-inflammatory effect of lemon and hot pepper extracts on adjuvant-induced arthritis in mice. J Basic Appl. Zoo. 67: 149–157.
Wheeler, G., Ishikawa, T., Pornsaksit, V., Smirnoff, N. 2015. Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. Elife 4: 2104–2105.
Wheeler, G., Ishikawa, T., Pornsaksit, V., Smirnoff, N. 2015. Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. Elife 4: 2104–2105.
Zeb, A., Imran, M. 2019. Carotenoids, pigments, phenolic composition and antioxidant activity of Oxalis corniculata leaves. Food Biosci. 32: 1–9.
Zhao, Y., Zhang, M., Yang, W., Di, H.J., Ma, L., Liu, W., Li, B. 2019. Effects of microbial inoculants on phosphorus and potassium availability, bacterial community composition, and pepper growth in a calcareous soil: a greenhouse study. J Soils Sediments. 19: 3597–3607.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
The journal Biotecnia is licensed under the Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) license.