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Revista mexicana de ciencias agrícolas
versión impresa ISSN 2007-0934
Rev. Mex. Cienc. Agríc vol.15 no.2 Texcoco feb./mar. 2024 Epub 21-Jun-2024
https://doi.org/10.29312/remexca.v15i2.3638
Articles
Benzoic acid improves nutritional quality in lentil sprouts
1Tecnológico Nacional de México-Instituto Tecnológico Superior de Lerdo. Av. Tecnológico núm. 1555, Sur Periférico Gómez-Lerdo km 14.5, Lerdo, Durango, México. (ale.gaucin@gmail.com).
2Tecnológico Nacional de México-Instituto Tecnológico de Torreón. Carretera Torreón-San Pedro km 7.5, Torreón, Coahuila, México. (selenne.mg@torreon.tecnm.mx).
3Universidad Autónoma de Nuevo León-Facultad de Agronomía. Av. Francisco Villa s/n, exhacienda el Canadá, General Escobedo, Nuevo León, México. CP. 66450 (fcarballom@uanl.edu.mx).
4Universidad Autónoma Agraria Antonio Narro-Unidad Laguna. Periférico Raúl López Sánchez s/n, Colonia Valle Verde, Torreón, Coahuila, México. CP. 27054. (alejamorsa@hotmail.com).
5Universidad Tecnológica de Escuinapa, Camino al Guasimal s/n, colonia Centro, Escuinapa de Hidalgo, Sinaloa, México. CP. 82400. (berna-palomeque@outlook.com).
6Universidad Politécnica de Gómez Palacio. Carretera El Vergel-La Torreña km 0 820, El Vergel, Gómez Palacio, Durango, México.
Sprouts are foods that have been winning consumers for their pleasant freshness and are used to accompany various dishes, both at home and in a large number of restaurants around the world. In addition, they represent a food of high nutritional quality since they are a source of minerals, vitamins, and bioactive compounds. The use of elicitors can improve the nutritional quality of these foods. In this study, five concentrations (0, 10-2, 10-3, 10-4, and 10-5 M) of benzoic acid were evaluated in lentil (Lens culinaris L.) sprouts. Biomass production, total soluble solids, total phenolic compounds, total flavonoids, and total antioxidant capacity were quantified. Elicitation with BA at low concentrations significantly improved the accumulation of DM and bioactive compounds; on the other hand, high concentrations significantly reduced these parameters. Elicitation with BA is a simple and efficient alternative to promote biomass production and induce the biosynthesis of bioactive compounds in lentil sprouts to obtain functional foods.
Keywords: Lens culinaris L.; elicitors; nutritional quality.
Los brotes o germinados son alimentos que han ido conquistando a los consumidores por su agradable frescura y se usan acompañando a diversos platos, tanto a nivel doméstico como en un gran número de restaurantes de todo el mundo. Además, representan un alimento de alta calidad nutricional, debido a que son fuente de minerales, vitaminas y compuestos bioactivos. La utilización de elicitores puede mejorar la calidad nutricional de estos alimentos. En este estudio se evaluaron cinco concentraciones (0, 10-2, 10-3, 10-4 y 10-5 M) de ácido benzoico en germinados de lenteja (Lens culinaris L.). Se cuantificó la producción de biomasa, sólidos solubles totales, compuestos fenólicos totales, flavonoides totales y la capacidad antioxidante total. La elicitación con AB en bajas concentraciones mejoró significativamente la acumulación de MS y compuestos bioactivos; en cambio altas concentraciones redujeron significativamente estos parámetros. La elicitación con AB es una alternativa simple y eficiente para promover la producción de biomasa e inducir la biosíntesis de compuestos bioactivos en germinados de lenteja, para obtener alimentos funcionales.
Palabras clave: Lens culinaris L.; calidad nutricional; elicitores
Introduction
Elicitors are substances from various sources, both inorganic and organic, which, when applied exogenously to plants, trigger various physiological modifications, and stimulate the plant’s defense mechanisms against biotic or abiotic stress (Salifu et al., 2022). Biotic elicitors are all those substances generated by living organisms, such as proteins, carbohydrates, bacteria, fungi, and phytohormones.
On the other hand, abiotic elicitors are all the physical stimuli to which plants are susceptible, such as light, temperature, long-distance electrical signals, electromagnetic waves, radio frequency waves, perception of mechanical stimuli, and acoustic emissions, among others. These substances act as plant signalers by inducing the production of reactive oxygen species (ROS) that stimulate the plant to produce defense mechanisms such as hormones, antioxidants, enzymatic and non-enzymatic, in order to mitigate the effects of ROS (Da Silva et al., 2023).
Benzoic acid (C7H6O2) is an aromatic carboxylic acid that has a carboxyl group attached to a phenolic ring; it is produced naturally in plants. Its exogenous application as an elicitor produces an increase in the content of bioactive compounds in plants and plays important roles in the biosynthesis of phenylpropanoid compounds, which are precursors of a wide range of primary and secondary metabolites, such as phenolics and flavonoids (Tena et al., 2021).
These function as cellular antioxidants and inhibit ROS (Marchiosi et al., 2020); they also prevent the beginning of degenerative diseases (Rai et al., 2021; Koza et al., 2022) as they help mitigate the damage caused by oxidative stress and the loss of the antioxidant regulatory system (Ahmed et al., 2022; Monib et al., 2023). On the other hand, sprouts are a source of carbohydrates, fiber, vitamins, essential nutrients, and bioactive compounds, which have been linked to disease prevention and treatment (Lemmens et al., 2019; Ebert et al., 2022).
The germination process makes it possible to obtain grains with high biological activity after enzymatic hydrolysis, thus enabling the accumulation of bioactive compounds (Choque-Quispe et al., 2020), which improves antioxidant activity (Pathan et al., 2022; Salifu et al., 2022). Sprouted lentils have better nutritional properties than seeds (Bautista-Expósito et al., 2021; Rico et al., 2022).
The content of vitamins, minerals, trace elements, and enzymes can multiply exponentially during germination (Galieni et al., 2020). The fresh consumption of lentil sprouts provides carbohydrates, fiber, vitamins, nutrients, and a high content of phytochemical compounds with bioactive effects, such as antidiabetic, anti-inflammatory, anticancer, antihypertensive, and antioxidant activity (Hernández-Aguilar et al., 2020; Miyahira et al., 2021).
These properties are due to the action of bioactive compounds, so their increase in sprouts is a line of research for obtaining functional foods (Kumar et al., 2022). Sprouts are widely accepted in the market, especially by people who cannot consume foods of animal origin (Waliat et al., 2023). They are usually easy to digest (Galanty et al., 2022; Ponce de León et al., 2022).
The use of BA during the sprout production period could be a very useful tool to enhance the synthesis of bioactive compounds. Based on the above, this research aimed to evaluate the effect of the application of benzoic acid on the content of bioactive compounds in lentil sprouts.
Materials and methods
Plant material and germination conditions
The research was carried out in a Food Biotechnology Laboratory of the Polytechnic University of Gómez Palacio, located in the city of Gómez Palacio, Durango. Lentil seeds from the company Aires de Campo were used, with a minimum germination percentage of 97%. The seeds were weighed on an analytical balance (Ohaus Adventurer®) in a proportion of 5 g; they were subjected to washing by immersion in drinking water containing sodium hypochlorite (NaClO) at a concentration of (1 ml L-1) at a temperature of (18 °C) for 15 min to eliminate harmful agents that it may contain; the seeds were rinsed with drinking water twice to remove excess NaClO; they were also left to drain for two minutes to minimize excess water before pregermination, which consisted of immersion of the seed in drinking water at 18 °C for 6 h (Dziki et al., 2015).
The germination stage consisted of placing the pregerminated seeds in the basal part in foamed polystyrene trays (15 x 10 x 5 cm) in germination paper (Tlymopukt®), with perforations in the basal part to allow sufficient aeration and avoid the proliferation of harmful agents; these trays were placed in darkness at room temperature (20 °C) for 6 h. After this time, the growth stage began, which consisted of placing the trays on shelves with natural lighting for six days.
Treatments, experimental design
Distilled water was irrigated in the germination and growth stages every 3 h by sprinkling with a dose of 5 ml per application. The treatments were applied in the same irrigation and consisted of the application of C7H6O2 (Sigma-Aldrich, USA, 99%) in the following concentrations: 0, 10-2, 10-3, 10-4, and 10-5 M. The experimental design used was completely randomized, with nine repetitions per treatment.
Variables evaluated
To assess the treatments, the following variables were measured: percentages of dry matter (DM), total soluble solids (TSS), total phenolic compound (TPC) content, total flavonoids (TF), and total antioxidant capacity (TAC). Dry matter was determined following the AOAC (1990) methodology. To determine the total soluble solids (TSS), 2 g of the sprouts was weighed, macerated in a mortar with a pestle, and a few drops of the macerated were placed in the prism of a manual refractometer (Atago Master 53M).
Obtaining extracts
To obtain extracts, 2 g of fresh sample was mixed in 10 ml of 80% ethanol in glass tubes with screw caps, which were placed in a rotary stirrer (ATR Inc., USA) for 24 h at 20 rpm at 5 °C. The tubes were then centrifuged at 3 000 rpm for 5 min; the supernatant was extracted for further analysis.
Bioactive compounds
Total phenolic compounds: total phenolic content was determined by the Folin-Ciocalteau method (Sariñana-Navarrete et al., 2021). Samples were quantified on a UV-Vis ultraviolet spectrophotometer at 760 nm (GENESYS 10S UV-Vis, Thermo Fisher Scientific, Inc., MA, USA). The standard was prepared with gallic acid. Results were expressed in mg GAE 100 g-1 fresh weight (FW).
Total flavonoids: total flavonoids were determined by colorimetry (Sariñana-Navarrete et al., 2021). Samples were quantified on a UV-Vis spectrophotometer at 510 nm (GENESYS 10S UV-Vis, Thermo Fisher Scientific, Inc., MA, USA). The standard was prepared with quercetin dissolved in absolute ethanol (y= 0.0122x -0.0067; r2= 0.965). Results were expressed as mg QE 100 g-1 FW.
Total antioxidant capacity: total antioxidant capacity was measured using the in vitro method of DPPH+ (Brand-Williams et al., 1995). Samples were quantified on a UV-Vis spectrophotometer at 517 nm (GENESYS 10S UV-Vis, Thermo Fisher Scientific, Inc., MA, USA). The standard was prepared with Trolox (0.1-1 mM, r2= 0.998). The results were expressed as μM Trolox equivalents 100 g-1 FW.
Statistical analysis
In order to comply with the assumptions of normality and homogeneity of the variances of the dry matter percentage data, these were transformed using arcsine, and subsequently, the results obtained were subjected to a simple classification analysis of variance and post hoc multiple comparison of means using the Tukey HSD test at a probability of 5%, with SAS v 9.0 software.
Results and discussion
The use of BA caused significant differences in the DM content in lentil sprouts (Figure 1). The concentration of 10-2 M exceeded the control treatment by 8%, and the concentration of 10-5 M decreased by 10%. The results indicate that the application of BA in high concentrations causes a decrease in the accumulation of dry matter in sprouts in response to stress, as reported by (Salas-Pérez et al., 2016).
Figure 1 Dry matter and total soluble solids in lentil sprouts under different molar concentrations of benzoic acid. Means with the same literal are not significant according to Tukey (p< 0.05).
These researchers indicate that high doses of elicitors cause stress, which causes decreases in cell division and in the synthesis of auxins or cytokinins. Several studies show the effect of BA in high concentrations, such as the study by Valdez-Sepúlveda et al. (2015), they report that BA in high doses decreased the accumulation of fresh biomass in Solanum lycopersicum. Prado et al. (2012) indicate that the application of BA decreased the accumulation of fresh biomass in (Lactuca sativa).
Therefore, this effect could be attributed to the fact that BA interacts in the metabolic activity of the seed and inhibits certain physiological processes and translocation of metabolites that interfere with growth. On the other hand, it has been reported that in low doses of elicitors, such as BA, it induces plant resistance against pathogens by activating signals that enhance the production of secondary metabolites (Marchiosi et al., 2020), and participates in developmental signaling cascades that control the growth process (Abdul et al., 2020; Cherepanov and Zhuravleva, 2021).
The TSS in lentil sprouts showed differences between the different concentrations of BA used; the values obtained fluctuated between 9 and 12 °Brix. The concentration of 10-2 M exceeded the control treatment by 27%, and the concentration of 10-5 M decreased by 19% compared to the concentration of 10-2 M. The observed change in TSS indicates that BA tends to modify the physiological state of sprouts due to the translocation and accumulation of metabolites in the tissue, which can lead to a higher concentration of starch in glucose (Salas et al., 2018).
This is because when BA exerts a network that involves parallel pathways that cross distributed through multiple subcellular compartments, it allows the volatile compounds of benzoyl (derived from BA), benzyl (derived from benzyl alcohol), and anthraniloyl (obtained from anthranilic acid) to function as aroma and flavor compounds (Widhalm, 2015).
On the other hand, several studies have shown that the use of elicitors in low concentrations causes an increase in TSS because their use causes stimulation and accumulation of metabolite synthesis (Luo et al., 2020; Saravanakumar et al., 2022). This was examined in sprouts of Chenopodium quinoa Willd, Triticum spp. (Salas Pérez et al., 2018), Solanum nigrum L. (Bano et al., 2019), Papaver rhoeas L. (Senila et al., 2020), Cucumis sativus L. (Cherepanov and Zhuravleva, 2021), and Lens culinaris L. (Debeski et al., 2021).
Conversely, high doses of BA affect plant metabolism by unbalancing the flow of electrons through the electron transport chain, causing the production of superoxide radicals and singlet oxygen (Benincasa et al., 2019). This is probably due to the overexposure of the element that emits high-intensity stress, which caused alterations in the physiological system of the sprouts since, during seed imbibition, the controlled generation of ROS is involved in the perception and transduction of the environmental conditions that control germination (Bailly, 2019).
In relation to bioactive compounds, it was shown that BA can act as an agent inducing metabolic processes since they can increase the content of bioactive compounds important in the development and stimulating effect of the production of secondary metabolites (Waqas et al., 2019; Marchiosi et al., 2020). The results showed that the use of BA causes differences in phenolic compounds and flavonoids, as well as antioxidant capacity (Figure 2) in lentil sprouts.
Figure 2 Total phenolic compounds, total phenols, and total antioxidant capacity in lentil sprouts under different molar concentrations of benzoic acid. Means with the same literal are not significant according to Tukey (p< 0.05).
Low doses of BA increased the content of phenols and flavonoids by 28% and 24% compared to the control, which corroborated the positive effect of BA on lentil sprouts. Such results can be attributed to the fact that low concentrations of BA induce metabolic components that perform critical functions in plants (Widhalm et al., 2015; Del Mundo, 2021). This significantly alters the biochemical composition and functionality of legume sprouts and seeds (Fouad et al., 2015; Debeski et al., 2021).
The content of phytochemical compounds in plants depends on stressful growing conditions (Ramírez-Estrada et al., 2016; Gaikwad et al., 2022; Kumar et al., 2023). In recent years, reports have been published on the effects of various elicitors on sprout composition (Benincasa et al., 2019; Cherepanov and Zhuravleva, 2021).
Soaking seeds in solutions containing organic acid compounds in low concentrations has also been shown to increase the content of phenolic compounds in legume sprouts (Dębski et al., 2021) and phenylpropanoid compounds in Triticum sprouts (Salas-Pérez et al., 2018). The use of BA during seed germination is an alternative to increase the activity of antioxidant enzymes and the content of phenolic compounds and, therefore, flavonoids (Valdez-Sepúlveda et al., 2015; Sachdev et al., 2021).
BA can lead to H2O2 synthesis (Wildermuth et al., 2006; Godoy et al., 2021; Dias et al., 2021), also increasing the synthesis of plant defense enzymes, such as polyphenols, flavonoids, and phytoalexins (Sharma et al., 2019; Liu et al., 2021), enhancing defense responses to biotic and abiotic stress (Nabavi et al., 2020; Aloo et al., 2021).
The use of elicitors may be a viable alternative to improve the nutritional quality of sprouts (Ramírez-Estrada et al., 2016; Benincasa et al., 2019); nevertheless, it is difficult to pinpoint the effects of BA on the content of bioactive compounds in sprouts as it depends on stressful growing conditions, plant species, growth stages, dosage, and exposure (Kapoor et al., 2020).
In relation to antioxidant capacity, the different concentrations of BA caused a significant difference in lentil sprouts; values ranging from 98 to 115 μM Trolox equiv 100 g-1 FW were obtained (Figure 2c). The highest antioxidant capacity was found in Triticum sprouts with a concentration of 10-2 M, while high concentrations and control treatment showed the lowest antioxidant activity.
High concentrations of BA reduce the antioxidant capacity of lentil sprouts. High doses of BA can cause oxidative stress and decrease antioxidant biosynthesis (Deng et al., 2017) due to the high production of ROS species through the shikimate/chorismate pathway and phenylalanine Phe (Valdez-Sepúlveda et al., 2015).
This explains the reasons why BA modifies the growth, stress tolerance, anatomy, and morphology of plant species (Yoo et al., 2013) since elicitors in high concentrations generate a breakdown of normal cell function, as well as physiological and morphological damage in different macromolecules, causing irreversible damage to lipids, nucleic acids, and cellular proteins (Marchiosi et al., 2020; Aguirre-Becerra et al., 2021).
Conclusions
The application of benzoic acid improves the nutritional quality of lentil sprouts. Low concentrations of benzoic acid significantly increase the production of biomass, total soluble solids, and bioactive compounds; conversely, high concentrations cause a negative effect.
The application of benzoic acid in low concentrations induces secondary metabolism in the germination stage and is effective in stimulating the biosynthesis of bioactive compounds, thus expanding the possibilities of the use of functional foods as an alternative to increase the nutritional quality of lentil sprouts.
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Received: January 01, 2024; Accepted: March 01, 2024
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