Changes in folic acid,phenolic components,and angiotensin-converting enzyme inhibitory activity in cowpea ( Vigna unguiculata ) green pods with different pod maturity

Abstract

Objective:

Cowpea is an important dry bean in developing countries, and its young leaves and green pods are consumed as fresh vegetables. Consuming green pods provides vitamins, minerals, and functional components for small-scale farmers with limited access to vegetables. However, the accumulation process of functional components in young cowpea pods is unknown. Therefore, we evaluated the concentrations of folic acid, phenolic components, and angiotensin-converting enzyme (ACE) inhibitory activity in green pods throughout maturity to determine the accumulation process of functional components.

Methods:

Four cowpea genotypes were selected from a mini-core subset of the world cowpea germplasm collection based on protein content, seed size, and seed coat color. The accumulation process of functional components in young cowpea pods was evaluated by measuring the concentrations of folic acid, phenolic components, and ACE inhibitory activity in green pods throughout pod growth (10 days after flowering (DAF): pod elongated, 15 and 20 DAF: seed growth, and 25 DAF: ready for harvest).

Results:

Our results demonstrate that consuming green cowpea pods during the early growth stages (10–15 DAF) can simultaneously provide a high content of dual nutrition, folic acid, and phenolic components. In addition, the pod had high ACE inhibitory activity. Folic acid and phenolic components were highest in the early stages of 10 DAF, whereas ACE inhibitory activity remained constant during 10–25 DAF.

Conclusion:

Our findings suggest that including green cowpea pods in diets can boost folic acid and phenolic component intakes without disrupting the ACE inhibitory activity. Furthermore, underutilized genetic resources featuring colored seeds would enhance the nutritional value of cowpeas in breeding programs, thereby increasing the nutritional benefits derived from cowpea consumption.

Keywords

Food crop genetic diversity grain legume West Africa young cowpea pod

Introduction

Cowpea (Vigna unguiculata [L.] Walp.) is a heat and drought-tolerant annual legume originating in Africa and extensively cultivated in America, Asia, and Europe. In West Africa, cowpea is important for regional food security. Cowpea seed has a relatively low fat content and high total protein content, similar to other pulses.¹ While cowpeas are mostly grown for their edible seed, their young leaves and green pods have also been utilized as fresh vegetables.² Cowpeas are not only an excellent source of protein and energy but also have numerous health-promoting components. Carvalho et al. (2022) evaluated protein, minerals, and phenolic contents for immature pods at the full elongation stage and revealed higher contents in the immature pods than in mature grain.³ The consumption of young green cowpea pods may improve intake of those nutritional/health-promoting components with minimal cooking time because the pods are softer than mature seeds, thereby minimizing nutrient loss during heat treatment.^4,5

Cowpea pods generally take approximately 30 days after flowering (DAF) to mature fully. For green pod consumption, the timing of pod harvesting is crucial to ensure optimal nutrient intake. Our previous study revealed that consumption of green pods at the early growth stage, before 10 DAF, did not contribute to protein intake.⁶ Also, there are limited previous studies on the content of other nutrients, minerals, fat and vitamins at young pod,^1,3,4,7 nutrient and/or health-promoting components content other than the protein would also be different for the pod growing stages. Additionally, cowpea contains several functional components such as phenolic components and angiotensin-converting enzyme (ACE) inhibitory substance.^1,7 These components are not nutrition, but also considered beneficial to human health as health-promoting components.^8–13 However, the accumulation process in different pod-growth stages has been rarely compared, particularly of functional components, such as folic acid, phenolic components, and ACE inhibitory activity in green pods. Clarifying the accumulation process of these components during pod growth is essential in understanding how green pod consumption affects nutrient/functional components intake.

This study evaluated temporal changes in folic acid, phenolic components, and angiotensin-converting enzyme (ACE) inhibitory activity in green pods at different growth stages to assess the optimal time for consumption. Genetic resources with different seed colors were used to compare nutrient accumulation for cowpea genotypes. Genetic resources with colored seeds are often eliminated during the selection phase in breeding programs due to strong consumer preferences in West Africa.^14,15,16 However, accumulation process of nutrient and/or health-promoting components in colored seed genotypes would be important information, unfolding its utilization in breeding programs especially targeted for green pod consumption.

Materials and methods

Plant materials and growth conditions

Four cowpea genotypes were selected from a mini-core subset of the World Cowpea Germplasm Collection of the International Institute of Tropical Agriculture (IITA).¹⁷ Genotype selection was based on the protein content and seed size evaluation data from a database (https://www.jircas.go.jp/en/database). TVu2168 and TVu3076 genotypes had small seed sizes of 6.9 g and 8.0 g per hundred seed weight and high and low protein contents of 22.8% and 18.3%, respectively. Conversely, TVu3282 and TVu4535 cowpea genotypes had relatively large seed sizes of 14.4 g and 15.2 g per hundred seed weight, respectively. These genotypes also differed in protein content, with TVu3282 showing a higher protein content of 22%, while TVu4535 had a lower protein content of 18.6%. The four genotypes exhibited similar flowering dates and phenotypical traits. The seed base colors of TVu2168, TVu3282, and TVu4535 genotypes were brown, whereas that of TVu3076 was cream.

The plants were grown in an experimental field at IITA in Ibadan, Nigeria (7°29ʹN, 3°54ʹE). The soil at IITA is sandy loam with moderate acidity (pH 5.8–6.1). Seeds were sown in early September 2022 in five rows in a plot 8 m long, with 20 cm in-row spacing on ridges 1.5 m apart. Weeding was performed manually, as required. No fertilizers were applied in this study. The total precipitation and average maximum and minimum temperatures for the growing period were 401 mm, 29.4 ± 2.6, and /22.6 ± 0.9 °C, respectively. No water stress or nutrient deficiency symptoms were observed during the growth period.

Pod and seed sampling

For the sampling, 150 peduncles were randomly selected at the flowering stage from each genotype (about 30 peduncles were selected from the 10 plants with 5 replicates). The peduncles of plants exhibiting uniform growth were selected. The date of the first flowering on a peduncle was tagged and recorded as the day of the year. The time lags of the flowering date among the flowers per peduncle were small; therefore, they were not considered. The pods from each peduncle were sampled 10, 15, and 20 DAF as green cowpea immature pods and at 25 DAF as mature pods. The sampling dates were based on the results from our previous study, which revealed that seed protein accumulation begins at 10 DAF when pod elongation is almost complete.¹⁴ At 10, 15, 20, and 25 DAF, 30, 15, 10, and 10 pods were sampled from the 30 peduncles of each replication, respectively. Images of the pods at each sampling interval are presented in Figure 1.

Figure 1.

Green pods representing each development stage and their matured seeds. TVu2168 and TVu3076 are small-seed-size cowpea genotypes with high- and low-protein contents, respectively. TVu3282 and TVu4535 are large-seed-size cowpea genotypes with high- and low-protein contents, respectively. DAF: days after flowering.

The pods collected at 15, 20, and 25 DAF were separated into seeds and pod shell samples and then freeze-dried. The samples collected at 10 DAF were freeze-dried as whole-pod samples to avoid destruction during separation. The freeze-dried samples were weighed and stored at −20 °C until nutrient analysis.

Folic acid content evaluation

Folic acid content was determined using a quantification kit (VitaFast Folic acid; Institut für Produktqualität GmbH, Munich, Germany). A ground freeze-dried sample (200 mg) was used for extraction in 10 mL of phosphate buffer at 37 °C overnight. The extracted solution was assessed according to the standard kit protocol, and the absorbance was measured at 620 nm using a microplate reader (ChroMate4300; Awareness Technologies, Palm City, FL, USA) with Windows software (ChroMate Manager version 6.3.1.263, Awareness Technology, Palm City, FL, USA). The folic acid content was determined as µg/100 mg of freeze-dried sample.

Determination of total phenolic content

A ground freeze-dried sample (100 mg) was used for extraction in 1.0 mL of ethanol/distilled water (70:30, v/v).^18,19 After adding the 70% ethanol, the sample was vortexed and incubated at room temperature (21‒26 °C) for 15 min. The mixture was centrifuged at 1610 xg for 15 min, and the supernatant was recovered. The extraction process was conducted twice. A 10-µL extract sample was mixed with 75 µL Folin-Ciocalteu reagent and shaken for 1 min. Subsequently, the mixture was left for 5 min, after which 75 µL of 2% sodium carbonate solution was added and shaken for 1 min. After 15 min, the absorbance was measured at 750 nm using the microplate reader with Windows software. The absorbance of the reaction using water instead of the extract or standard was subtracted from that of the reaction with the sample. Gallic acid dilutions (0.01–0.5 mg/mL) were used as standards for calibration. The total phenolic content was expressed in mg of gallic acid equivalent per 100 g of freeze-dried sample (mg GAE/100 g).

Evaluation of ACE inhibitory activity

ACE inhibitory activity was evaluated using an ACE Kit-WST (Dojindo EU GMbH, München, Germany; Dojindo Laboratories, Kumamoto, Japan). A 2 g ground freeze-dried sample was used for extraction in 10 mL of distilled water at room temperature (21‒26 °C) overnight. Subsequently, extraction was continued in a boiling water bath for 60 min. After centrifugation at 1118 xg for 15 min, the supernatant was filtered using a 0.2-µm cellulose acetate filter membrane (Thermo Fisher Scientific, Waltham, MA, USA). The extracted solution was yellowish and was processed following the protocol for colored samples using the ACE Kit-WST (Amerigo Scientific Inc., Pocatello, ID, USA). The absorbance at 450 nm was measured using the microplate reader with Windows software.

Statistical analysis

Tukey's multiple comparison test was performed to detect significant differences in dry weight, folic acid concentration, phenolic component concentration, and ACE inhibitory activity among sampling dates and sample parts. All analyses were performed using the statistical software R version 4.2.2 (RStudio, Boston, MA, USA).

Results

The results revealed that seed weight increased with time, whereas pod weight remained constant (Figure 2A, also see supplemental Table S1). In TVu2168, TVu3076, and TVu3282 genotypes, seed enlargement was almost complete at 20 DAF; however, TVu4535, which had the largest seed size, exhibited a significant increase in seed size after 20 DAF. In all cases, total pod weight was attributed to an increase in seed weight, while pod weight remained almost unchanged.

Figure 2.

Changes in the nutritional components with pod growth of each genotype. The values of total pod (gray circle), pod-shell (green triangle), and seeds (red square) were separately shown at different growth stages (10, 15, 20, and 25 DAF). Each point represents the mean ± standard deviation of the five replications. (A) Dry weight of single pod or seed weight. (B) Folic acid concentration (µg 100g⁻¹) of pods or seeds. (C) Concentration of phenolic compounds in pods or seeds. (D) Angiotensin-converting enzyme (ACE) inhibitory activity (Final concentration of the extract was 15.4 mg ml⁻¹).

At 10 DAF, folic acid accumulated at high concentrations in the total pod base of the four genotypes (Figure 2B). At 15 DAF, folic acid concentration in the pod shell was higher than in the seed. However, it significantly decreased as the pods matured, reaching a lower level at 25 DAF. Folic acid concentration in the seeds increased from 10 to 25 DAF in TVu2168, whereas no significant changes were observed in the other genotypes. At 25 DAF, folic acid concentrations were higher in the seeds than in the pod shells for all genotypes except TVu3076. In addition, the concentration of folic acid in the seeds slightly increased during the development stages and decreased in the pods in all genotypes.

Changes in the concentration of phenolic components were similar among the genotypes (Figure 2C). The concentration of phenolic components was the highest at 10 DAF in whole pod bases and the lowest in pod shells and seeds after 15 DAF. A higher concentration of phenolic components was observed in TVu2168 and TVu4535 at 10 DAF than in the other genotypes. The concentrations of phenolic components in the pod shells and seeds decreased from 15 to 25 DAF. For TVu3076 and TVu3282, the concentration of phenolic components was lower in seeds than in pod shells.

ACE inhibitory activity was higher in the seeds than in the pod shells throughout the maturity period (Figure 2D). Although the changes in seeds and pod shells after 15 DAF were not statistically significant, they were highly dependent on the genotype. The ACE inhibitory activity in seeds increased in TVu2168 and TVu3282, whereas it decreased in TVu3076. ACE inhibitory activity in the pod shell decreased in all genotypes except for TVu3282.

Discussion

This study assessed nutrient quality based on concentration/activity rather than total content per pod. This approach is more relevant for discussing the nutritional quality of young green pods because it focuses on the intake per meal rather than the total content of a single pod. Naturally, early-stage seeds are smaller than mature seeds in terms of dry weight (Figure 2B), but the concentration of folic acid and phenolic components was higher than in later periods. Folic acid concentration was maintained at approximately 600‒800 µg/100 g at 10 DAF, which was much higher than the natural variation of folic acid content in matured seeds (177‒780 µg/100 g).²⁰ A similar tendency was observed for phenolic compounds, consistent with previous reports that the concentration in immature pods is, on average, five times higher than that in mature ones.²¹

Time-course changes in each nutritional component varied. Particularly, the concentrations of folic acid and phenolic components were highest in the early stage of pod morphosis, regardless of the final seed size. Our results demonstrate that eating green pods during the early stages (10–15 DAF) can simultaneously provide high concentrations of dual nutrition, folic acid, and phenolic components. Although more pods and seeds were required than that of the other DAF samples if the mass consumed was similar, young green cowpea pods contained more folic acid and phenolic components.

The ACE inhibitory activity was almost the same during that period. The ACE inhibitory activity of legumes is derived from peptides such as nicochianamine.^22,23 Although the concentration and content of ACE inhibitory substances in the samples were not evaluated because the ACE inhibitor of cowpeas has not been identified, the inhibitory activity was nearly similar from pod formation to seed development. Thus, nearly uniform ACE inhibitory activity is expected to be attained by consuming green cowpea pods and seeds after 10 DAF.

Folic acid is synthesized in the mitochondria and accumulates in the vacuoles, and part of it decomposes and is used for resynthesis.²⁴ Natural folic acid (folate) is unstable to varying degrees, considering oxidative cleavage.²⁵ Therefore, folic acid concentration was the highest at the beginning of pod formation and decreased with pod elongation and exposure to ultraviolet light. The concentration of folic acid in the seeds slightly increased during the development stages and decreased in the pods. Although there are limited reports on the transportation and turnover of folic acid in plant tissues,^18,26 the drastic decrease in folic acid concentration in the pods suggests the transfer of folic acid (or its precursor) from the pods to the seeds. Additionally, the pods could protect folic acid in the seeds and become relatively stable or increase. Measurements of tomato fruit folate have shown a decrease during ripening, and substantial decreases have also been reported for strawberries, spinach, and peas during postharvest storage.^18,26,27 Whether this decline is enzymatic or due to chemical breakdown as endogenous antioxidants are depleted remains unclear. Hence, the early stages of green pod formation are considered preferable for high folic acid intake.

The variation ranges in the concentrations of the phenolic compound of mature seeds obtained in the current study (120‒239 mg/100 g) was relatively small compared to the previous study that evaluated 31 cowpea genotypes (63.14‒692.03 mg/100 g).²⁸ However, our results indicated that changes in concentration during pod growth were consistent for the genotypes with different final concentrations. Cowpeas have numerous phenolic components involved in various physiological functions.^29,30 For example, lignin, tannin, and other flavonoids are involved in defense against insects and fungi.^30–33 The decreasing concentration of phenolic components in the pods and seeds during the grain-filling period indicated that they are crucial in protecting pods during early development. After the initial synthesis of phenolic compounds, their concentrations in the pods and seeds decreased. Therefore, the phenolic compounds were probably not synthesized after providing the initial protective effect, after which their concentration per grain decreased with grain filling.

ACE inhibitory activity, which is derived from peptides such as nicotianamine, was slightly higher in seeds than that in pods. Nicotianamine is found in all plant organs and is involved in the detoxification and transport of iron, zinc, nickel, copper, and manganese as metal chelates.^34–36 Therefore, it is believed that nicotianamine accumulates as a metal chelate along with the transport of metal ions into seeds; thus, the ACE inhibitory activity in seeds was higher than that in pods.

Cowpeas with colored seed coats have a higher total flavonoid content than those with white seed coats.³⁷ Although most of the cowpea seed color begins to appear at approximately 15 DAF when grain enlargement is completed,³⁸ the concentration of phenolic components was highest at 10 DAF. These results suggest that the accumulation of phenolic components begins before grain enlargement. However, the correlation between folic acid (or ACE inhibitory activity) and seed color was not established. Most breeders in West Africa prioritize breeding lines with white seed coats owing to consumer preferences^15,16; Seed color does not influence the consumption of green cowpea pods or vegetable cowpeas. Furthermore, green cowpea pod consumption provides other nutrients, such as vitamins and minerals, which largely decrease before maturity.^4,39 Similar to the folic acid and phenolic components, these vitamins and minerals are available during the early stages of pod formation.^40,41 Furthermore, the sample size of this study was limited, the limited number of samples may affect the statistical significance of your results should also be taken into account in future analyses.

Conclusion

Our findings indicate that immature pods of early growth stage are suitable for consumption around 10 DAF, which increase folic acid and phenolic components intake without disrupting the ACE inhibitory activity. The accumulation processes of the investigated nutrients/health-promoting components were independent of seed color, indicating that genotypes with colored seeds can be considered valuable genetic resources for green pod consumption.

Supplemental Material

sj-pdf-1-sci-10.1177_00368504251320163 - Supplemental material for Changes in folic acid, phenolic components, and angiotensin-converting enzyme inhibitory activity in cowpea (Vigna unguiculata) green pods with different pod maturity

Supplemental material, sj-pdf-1-sci-10.1177_00368504251320163 for Changes in folic acid, phenolic components, and angiotensin-converting enzyme inhibitory activity in cowpea (Vigna unguiculata) green pods with different pod maturity by Haruki Ishikawa, Ryo Matsumoto and Kohtaro Iseki in Science Progress

Footnotes

Acknowledgments

We thank Ms. Adedoyin Oluwaseun Oyinda for technical support during seed nitrogen analysis and folic acid and ACE inhibitory activity evaluation. We also thank Ms. Aworinde Omolade Rhoda for evaluating the total phenolic content and Ms. Olajumoke Olaleye for assisting with field cultivation and seed sampling. We would like to thank Editage () for English language editing.

Authors’ contributions

Conceptualization, H.I.; methodology and formal analysis, H.I., R.M., and K.I.; investigation and field work, H.I., R.M., and K.I.; writing-original draft preparation, H.I.; writing-review and editing, H.I., R.M., and K.I.; project administration, H.I. and K.I.; funding acquisition, H.I. and K.I. All authors have read and agreed to the published version of the manuscript.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data availability

All data generated or analyzed during this study are included in this published article.

Ethical approval

The study did not require ethical approval.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was part of an international collaborative research project funded by the Japanese Ministry of Agriculture, Forestry, and Fisheries. It also formed part of a research program for the Japan International Research Center for Agricultural Sciences, “Development of soil and crop management technologies to stabilize upland farming systems for African smallholder farmers.”

ORCID iD

Haruki Ishikawa

Ryo Matsumoto

Kohtaro Iseki

Supplemental material

Supplemental material for this article is available online.

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