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Article

Potential Biopesticides from Seed Extracts: A Sustainable Way to Protect Cotton Crops from Bollworm Damage

by
Masoud Chamani
1,*,
Narjes Askari
2,
Reza Farshbaf Pourabad
3,
Ali Chenari Bouket
4,
Tomasz Oszako
5 and
Lassaad Belbahri
6
1
Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil 5619911367, Iran
2
Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz 5166616471, Iran
3
Department of Plant Protection, Faculty of Agriculture, Ege University, Izmir 35100, Türkiye
4
East Azarbaijan Agricultural and Natural Resources Research and Education Centre, Plant Protection Research Department, Agricultural Research, Education and Extension Organization (AREEO), Tabriz 5355179854, Iran
5
Department of Forest Protection, Forest Research Institute in Sekocin Stary, 05-090 Raszyn, Poland
6
University Institute of Teacher Education (IUFE), University of Geneva, 24 Rue du Général-Dufour, 1211 Geneva, Switzerland
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(1), 145; https://doi.org/10.3390/su16010145
Submission received: 29 October 2023 / Revised: 15 December 2023 / Accepted: 20 December 2023 / Published: 22 December 2023
Browse Figures
Review Reports Versions Notes

Abstract

:
In the current study, the inhibitory effect of extracts from Gramineae (wheat, barley, and corn) and Leguminosae (sophora, bean, and pea) seeds was studied on the digestive alpha-amylase activity in cotton bollworm (Helicoverpa armigera Hubner). The insect was bred on artificial food based on Vigna unguiculata in the greenhouse condition (26 ± 2 °C, 60 ± 10% (Relative Humidity), R.H., 16:8 (Light: Darkness), L: D). The extracts of wheat (95.2%), barley (84.6%), corn (73.8%), sophora (77%), Vigna unguiculata (52%), and pea (56.7%) significantly inhibited the alpha-amylase activity in H. armigera. Studying the impact of different fractions (obtained via deposition at various concentrations of ammonium sulfate salt) on the alpha-amylase enzyme activity demonstrated that in 0–30% fractions, wheat, barley, and sophora have the highest effect (95.26%, 94.65%, and 94.73%, respectively) compared to the other fractions. The inhibitory activities of 0–30% fractions of corn, bean, and pea were 83.3, 56.94, and 50.92%, respectively. In 30–50% fractions, the most effective ones were those of wheat and barley with the inhibitory activity of 79.7% and 82.9%, respectively. In addition, bean and pea fractions inhibited 25.2% and 27.5%, in that order. No significant inhibitory impact was detected in 50–70% or higher fractions. The investigation of the impact of pH values (i.e., 2, 4, 8, and 10) on the inhibition of the alpha-amylase enzyme activity introduced 8–10 as the optimum pH in H. armigera. Nanotechnology offers several ways to enhance plant-based pesticides, which are a solution for making plant extract usage more efficient. The exploration of plant-based pesticides, in conjunction with the incorporation of nanotechnology and other scientific fields, offers a wide range of prospects for further investigation.

1. Introduction

Nowadays, new safe methodologies have been applied to manage pest insects based on natural compounds or biomaterials. Concerning the adverse effects of conventional pesticides, safe methodologies are recommended in the pest management of different plant extracts. Studies revealed that plants or other organisms (e.g., animals, bacteria, Fungi, etc.) produce special components with inhibitory effects on pests [1,2,3]. Thanks to minimum or no harmful effects to the ecosystem, as well as their natural structures and sources, they have gained great attention. A well-known example is rotenone, the recognized insecticides extracted from several leguminous plants with electron transfer blocking activity from nicotine amide-adenine (NADH) to ubiquinone [4]. The natural compounds with insecticidal properties, “defensin”, has been primarily detected in Sorghum bicolor (L.) Moench. The extracted substances demonstrated an inhibitory effect on the α-amylase activity in Periplaneta americana L. and Schistocerca americana Drury. In contrast, defensin had no inhibitory effect on mammalian enzymes [5]. In addition, digestive enzyme inhibitors are the main plant defense strategy for eliminating insect pests’ feeding. For instance, alpha-amylase inhibitors (α-AIs) restrict carbohydrate digestion and affect the metabolic and biochemical processes in insects [6,7]. Moreover, the Ragi bifunctional inhibitor (RBI) that inhibits both insect and mammalian α-amylases is mostly present in cereals [8]. In total, the susceptibility of insect enzymes is 2–50 times greater than that of human salivary amylase (HSA) [9].
In most insects, alpha-amylase is introduced as a key digestive enzyme. Through evolution, the enzyme has been evolved to obtain maximum nutrient compounds from host plants to supply required energy for the whole life cycle of insects [7]. α-AIs proteins are primarily found in seeds and roots, which store starch in the plant as a defensive strategy against herbivores [10]. Starch, as a main source of energy in insects, is converted into oligosaccharides by α-amylases and afterward glucose by alpha-glucosidase [11]. Starch digestion is prevented by α-AIs through blocking the starch access to the enzyme-active sites [9]. A wide range of diversity in α-AIs have been recognized amongst various plant species which are specific, so that the enzyme inhibitor may belong to only one family [9]. α-AIs have been detected in various plants such as cereals (e.g., wheat, barley, and millets), legumes (e.g., kidney beans, black beans, red kidney beans, peanuts, and chickpeas), and amaranth [9,12,13]. One of the well-known isoforms of α-AIs is α-AI-1, detected in some plants, specially Phaseolus vulgaris L. (such as white, red, black kidney beans), was classified as an α-AI homologous to plant lectins [13]. Additionally, α-AIs, extracted from local cultivars of the common bean (P. vulgaris), demonstrated inhibitory activity against the amylases of the third and fourth instar larval extracts of rice moth (Corcyra cephalonica Stainton), a reduction in larval growth, and 100% mortality after 11 days. In contrast, any mortality was recorded in adult insects after 45 days of larval stage [14].
All enzymes have an optimal operation in special ranges of pH. Alpha-amylase works in a different span of pH (4–11) [11]; some operate at low pH in the gut environment (e.g., Tenebrio molitor L. α-amylase (TMA) and Human Pancreatic α-Amylase (HPA)) and some work at high pH, like lepidopteran α-amylase (e.g., Ephestia kuehniella Zeller α-amylase 3 (EkAmy3)). However, the lepidopteran digestive enzymes’ span is limited in alkaline pH (9.8–11.2) [15]. In the company of pH, all enzymes have an optimum temperature to operate well. Insect α-amylases have a wide temperature range (i.e., 30–60 °C) as well [16,17,18,19].
Helicoverpa armigera (Hubner), a worldwide polyphagous pest, causes devastating damage to numerous agricultural products and infests various economic crops (e.g., cotton, chickpea, tomato, tobacco, corn, sesame, hemp, sunflower, peanut, okra, soybean, and bean) [20,21,22]. At various development stages, the vegetative and reproductive parts of host plants (stem, leaf, flower, and fruit) can be attacked by the larvae [23]. Given the wide range of hosts that cotton bollworms can infest and the well-documented medicinal properties of the Sophora plant, which contains metabolites that effectively inhibit enzyme activity [24], along with the recognized significance of wheat and barley in possessing inhibitors of digestive enzymes in insects [25,26], there is a promising perspective that the metabolites derived from these plants can be utilized as a potential solution against cotton bollworm infestations. By harnessing the inhibitory properties of these plant metabolites, we may be able to develop effective strategies to control and mitigate the damage caused by cotton bollworms. This research examined the inhibitory potential of seed extracts of some Gramineae (wheat, barley, and corn) and legume plants (pea, sophora, and bean) on digestive alpha-amylase in H. armigera, besides the optimal pH for the highest performance of these extracts.

2. Materials and Methods

2.1. Insect Rearing; Helicoverpa Armigera

To create the colony, Helicoverpa armigera were obtained from the Department of Plant Protection (University of Tabriz, Iran). The insects were bred for four successive generations on artificial food based on cowpea with some modifications [27] in the greenhouse of the department under 26 ± 2 °C, 60 ± 10% RH and 16:8 (L:D) conditions.

2.2. Dissection and Extraction of the Alpha-Amylase Enzyme

Larvae of H. armigera (4th age) that were 24 h old were selected for dissection and extraction. Foremost, the larvae were kept in the freezer (−4 °C, 5 min) to make them numb. Then, after splitting their sides, their guts were separated, transferred into 5 mL microtubes containing phosphate buffer (pH = 7), then homogenized and incubated for 1 h. Finally, the samples were centrifuged (10,000 rpm, 4 °C, 10 min) and the obtained supernatants were collected for the enzyme assay [28].

2.3. Preparation of Various Plant Extracts and Fractions

The necessary seeds for the preparation of inhibitory extracts, including Wheat, Barley, Corn, Sophora, Bean, and Pea, were sourced from the East Azerbaijan Agricultural and Natural Resources Research and Training Center located in Tabriz, Iran. To prepare seed extracts, 30 g of flour made from each seed were mixed with 100 mL of sodium chloride solution (concentration 0.1%). The obtained mixture was mixed slowly on a magnetic stirrer for 90 min at room temperature, then centrifuged (10,000 rpm, 4 °C, 30 min). The resulting liquid was transferred into microtubes and kept in the freezer (80 °C) as the inhibitor extract to conduct studies [29,30].
Due to the difference in solubility of ammonium sulfate salt at different temperatures, 4 °C was utilized as a standard temperature to prepare different fractions. In this study, four concentrations (0–30%, 30–50%, 50–70%, and 70–80% in 10 mL of ammonium sulfate solution) were employed. The equation provided on the website EnCor Biotechnology Inc. (https://encorbio.com (access date: 11 June 2023)) was utilized to calculate the precise quantity of ammonium sulfate salt needed for each fraction. The following table (Table 1) presents the concentrations and corresponding amounts of ammonium sulfate salt used per 10 mL solution:

2.4. Investigation of Activity of Digestive Alpha-Amylase Enzyme

Alpha-amylase activity was measured using a special diagnostic kit (manufactured by Pars Azmoon, Tehran, Iran). On deposition, there is an EPS-G7 composition (Ethylidene-p-nitroPhenyl-malthoheptaoside). The light absorbance was measured (405 nm, 37 °C) using the auto analyzer (model Abbott Alcyon 300, Abbott Laboratories, Inc., Irving, TX, USA).

2.5. Measuring the Inhibitory Effect of Plant Extracts and Fractions on the Activity of the Alpha-Amylase Enzyme

Silano et al. [31] implemented a standardized approach for categorizing alpha-amylase inhibitors in plant extracts. In this procedure, a plant-derived compound is added to a buffer solution containing alpha-amylase, followed by thorough mixing. A specified period is then allocated to assess the inhibitory impact on the enzyme. Subsequently, the amylase activity after the inhibitor’s influence and the degree of inhibition are determined. According to the diagnostic kit’s instructions, for evaluating the inhibitory effects of different extracts on alpha-amylase enzyme activity, 200 µL of the enzyme sample with 200 µL of the plant extract and 100 µL of buffer (pH = 7) were incubated (10 min, 37 °C), and enzyme activity was measured using the auto analyzer.

2.6. Determination of the Total Protein Concentration in the Samples

The Bradford [32] method was used to determine the total protein concentration in the samples. Bovine albumin protein was used as a standard, then a standard curve was plotted and the protein concentration was determined. Using a spectrophotometer, studies were carried out at 595 nm.

2.7. Determination of pH Impact on the Inhibition of the Herbal Extracts

Various phosphate buffers were used to detect enzyme activities, which were adjusted to different pH values (2, 4, 8, and 10) using sodium hydroxide and hydrochloric acid. Subsequently, alpha-amylase enzyme activity was measured at 37 °C.

2.8. Statistical Analyses

The data statistical analysis was conducted using SPSS software (version 20), based on a completely randomized design (CRD). The Duncan Multiple Range Test (DMRT) was used to compare the mean values at a significance level of 0.01. Additionally, Excel (2013) was used for graphing, numerical calculations, and examining regression relationships. All experiments were carefully conducted in triplicate to ensure robust and valid findings.

3. Results

3.1. The Inhibitory Impact of Plant Extracts

The statistical analysis of the data showed that the inhibitory effect of the herbal extracts on alpha-amylase activity in H. armigera was significant at the 1% level (Table 2).
Figure 1 demonstrates the inhibitory effect of various plant seed extracts on alpha-amylase enzyme activity. Wheat, barley, and sophora seed extracts exhibit the highest inhibitory activity, while beans and peas have the lowest. No significant differences are observed between corn and sophora, as well as between corn and beans and peas.

3.2. Inhibition of Alpha-Amylase Activity in Helicoverpa armigera by Different Fractions of Seed Extracts (Wheat, Barley, Corn, Sophora, Bean, and Pea)

The result showed significant differences between the extracts of wheat, barley, corn, sophora, bean, and pea (Table 3).
The inhibitory effects of different fractions on alpha-amylase activity in H. armigera were investigated. Table 4 presents a detailed breakdown of the inhibitory effects observed.
As it was shown in Figure 2, the highest inhibitory effect was observed in the 0–30% fraction, indicating its potency in suppressing alpha-amylase activity. The 30–50% fraction ranked second in terms of alpha-amylase inhibition, while no significant difference was found between the inhibitory effects of the 50–70% and 70–80% fractions.
Further analysis of specific fractions revealed varying inhibitory effects across different plant extracts. For barley, the highest alpha-amylase inhibitory effect was recorded in the 0–30% fraction, followed by the 30–50%, 50–70%, and 70–80% fractions.
Similarly, wheat, corn, sophora, and pea fractions exhibited the highest inhibitory effects in the 0–30% fraction, with the 30–50% fractions ranking second. The 50–70% and 70–80% fractions did not show any significant difference in inhibitory activity.
In contrast, the impact of different fractions of the bean extract on digestive alpha-amylase activity in H. armigera demonstrated the highest inhibitory activity in the 0–30% fraction. Notably, no significant differences were observed across the three fractions (30–50%, 50–70%, and 70–80%) in terms of inhibitory effects (Figure 2).

3.3. The Effect of pH Variations on the Inhibition of Alpha-Amylase Activity in Helicoverpa armigera by Plant Extracts

The alpha-amylase inhibition properties of wheat, barley, corn, sophora, beans, and peas exhibited varying responses at different pH levels. The highest level of inhibition was observed within the pH range of 8 to 10. Conversely, no inhibitory effect was detected in any of the herbal seed extracts at a pH level of 2 (Figure 3).

4. Discussion

Plant extracts are used as natural alternatives to synthetic pesticides in pest management. They can exert their influence in a variety of ways, including repellency, toxicity, and growth control. Plant extracts that repel pests by emitting strong scents or tastes discourage bugs from feeding or laying eggs. Toxic plant extracts contain bioactive substances that affect the nervous system, enzyme action, or the cuticle of the insect, causing death or decreased function. Plant extracts that regulate growth disrupt hormonal balance or molting processes, leading to aberrant growth, sterility, or developmental stoppage [33].
Based on various studies, alpha-amylase inhibitory proteins can be divided into seven distinct groups based on their protein structure. However, the majority of these groups exhibit minimal or no inhibitory activity. Interestingly, two of these groups have been found to possess a dual function, effectively inhibiting both alpha-amylase and protease enzymes [34].
In the current study, wheat extracts indicated the highest inhibitory effects on the digestive alpha-amylase activity in H. armigera, due to the high potential of wheat in blocking alpha-amylase in a wide range of mammals and pests [9,12,13]. Barley extract had the second-greatest inhibitory impact on the enzyme. Afterwards, the extracts of corn, sophora, pea, and bean exhibited inhibitory impacts, respectively (Figure 1). According to Franco et al. [35], α-AIs are widely found in many plants, especially grasses and legumes, in line with the results obtained in this study. Sophora is a medicinal plant exploited in Chinese traditional medicine, with antioxidant and inhibitory properties. α-AIs of Sophora japonica L. exhibited 40% inhibition on human alpha-amylase [36]. Recent studies conducted on sophora plant seeds (Sophora alopecuroides L.) demonstrated the high potential of this plant for inhibiting the alpha-amylase enzyme [37]. In another study, methanolic extracts of aerial parts like flowers, leaves, roots, and stems of S. alopecuroides var. alopecuroides revealed high alpha-amylase inhibitory activity [38].
It has been demonstrated by Alfonso et al. that protein inhibitors derived from wheat have a significant inhibitory effect on alpha-amylase activity in butterflies. Wheat α-AIs inhibited (9–11%) the activity of sunn pest (Eurygaster integriceps Puton) alpha-amylase [39]. One of the extracted α-AIs from barley could deactivate the digestive alpha-amylase of Tenebrio molitor L. [40]. Le Berre-Anton et al. [41] identified an α-AI extracted from the seeds of Phaseolus vulgaris L. called αAl-1. Furthermore, a case study of enzyme inhibitors of the seed extract from Vigna unguiculata L. revealed up to a 50% decrease in amylolytic activity in larvae of Callosobruchus maculatus F [30]. The application of bean proteinaceous extract significantly diminished (40%) the alpha-amylase activity in Hypothenemus humpei Ferrari. Two inhibitors (α Al-1 and α Al-2), able to protect transgenic peas from pea weevil (Bruchus pisorum L.), have been extracted from beans with inhibitory effects on the alpha-amylase of B. pisorum, with higher activity reported for α Al-1 than α Al-2 [42]. The obtained results complying with the previous outcomes suggested that plant defense proteins could be used as powerful enzyme inhibitors to control insect pests. Therefore, Graminae plants and Legumes, rich sources of α-AIs for H. armigera, could be considered as genetic pools for transferring the aforementioned inhibitors to plants via genetic engineering in order to improve resistance against the pest. To give an illustration, transferring alpha-amylase inhibitor cDNA from Phaseolus vulgaris into Pisum sativum caused resistance to the pea weevil Bruchus pisorum. These types of transgenic plants are not nutritionally detrimental to humans, since cooking them removes the inhibiting effect [43].
Considering the extraction and purification of proteinaceous inhibitors, different techniques are applied, including electrophoresis, chromatography, the ion exchange method, and deposition in ammonium sulfate salt. Due to some constraints of electrophoresis and chromatography, the deposition method with some material, such as ammonium sulfate, is considerable. Using this approach, the ammonium sulfate salt separates proteins based on their changes in solubility. Researchers have exploited different ammonium sulfate salt fractions for the separation of proteins (enzymes and enzyme inhibitors). To give an illustration, Powers et al. [44] purified alpha-amylase from the seeds of V. ungiculata into fractions of 30–60%. Furthermore, Silva et al. [45] used a fraction of 100% ammonium sulfate and observed 70% alpha-amylase inhibitory activity on C. maculatus larvae. In addition, Elarbi et al. [46] used 0–20 and 20–60% concentrations of ammonium sulfate salt to purify the amylase in safflower seed, and more than 95% of the enzyme activity was obtained in fractions of 20–60%. Based on the obtained results, it can be concluded that the majority of the α-AIs have low solubility in water and were separated with the 0–30% concentration; to put it another way, the higher the salt concentration, the lower the total extract (containing inhibitors) and the inhibitory percentage. These results provide valuable insights into the inhibitory effects of various fractions on alpha-amylase activity in H. armigera. The 0–30% fraction consistently exhibited the highest inhibitory activity across different seed extracts, suggesting the presence of potent inhibitors. These findings contribute to the understanding of the potential application of seed extracts as natural inhibitors for controlling alpha-amylase activity in H. armigera. Further research is warranted to identify the specific bioactive compounds responsible for the observed inhibitory effects and to elucidate their mode of action. Understanding the mechanisms underlying the inhibitory activity can aid in the development of effective and sustainable pest management strategies.
Several reports pointed to the close relation between the herbal inhibitor features, particularly pH and the enzyme alpha-amylase activity. For instance, red bean extract exhibited the highest inhibitory activity on pig pancreatic alpha-amylase at pH 5.5 [44]. Furthermore, the proteinaceous alpha-amylase inhibitor of corn seeds exhibited maximum efficacy against Fusarium verticillioides Saccardo amylase at pH 7.0 [47]. In another research, Valencia-Jiménez et al. [48] studied the optimum pH of some plant proteinaceous inhibitors at 50 °C and indicated that pH 6.0 caused 70 and 87% inhibition in the activity of α-AIs extracted from Phaseolus coccineus L. and P. vulgaris at pH 6.0, of which the α-AI obtained from the amaranth hybrid had no efficiency on the alpha-amylase activity, while pH 9.0 caused the most effective performance (80% inhibition). In the same manner, at pH 5.0, the α-AI achieved by Triticale (T-αAI) demonstrated the highest inhibitory activity on Eurygaster integriceps Puton alpha-amylase [49]. Also, Esmaeily et al. [50] determined the optimum pH as 10 for the inhibitory activity of barley and amaranth seeds against the carob moth (Ectomyelois ceratoniae Zeller). In the last case, Bharadwaj et al. [51] reported that the most effective activity of α-AI extracted from Mucuna pruriens L. was shown at pH 6.9. It has been made clear that pH is one of the main factors affecting the interaction between enzymes and inhibitors. Since the gut pH of H. armigera is reported to be slightly alkaline (pH 8–10) [52], in the present study the highest inhibitory activity was detected in the pH range of 8–10. Therefore, a proper concentration of inhibitors in the gut of H. armigera with an alkaline pH could cause an acceptable level of inhibition. According to the consistency of the optimum pH in the insect gut, the optimum value for the alpha-amylase activity of the insect, and also for the inhibitor activity, have been reported in other studies [48,49,53]. Chamani et al. [54] conducted a prior study where they determined that the digestive enzyme activity of H. armigera reached its peak at an alkaline pH. This finding suggests that an alkaline environment is ideal for the optimal functioning of the digestive enzymes in this species. Based on the findings presented in the current study, it can be concluded that the alpha-amylase inhibitory activity of the tested plant extracts varied at different pH levels. The highest inhibition was observed within the pH range of 8–10, which aligns with the reported slightly alkaline gut pH of H. armigera. This suggests that achieving an acceptable level of inhibition in the insect’s gut requires both the proper concentration of inhibitor and an alkaline pH environment. These results are consistent with previous studies that have also reported the importance of pH in the interaction between enzymes and inhibitors. Therefore, understanding and optimizing the pH conditions are crucial factors in designing effective biopesticides against pests like H. armigera.

Application of Plant Extract, Benefits, and Limitations

There has been limited research on the use of plant extracts for pest control, particularly in cotton, a globally significant crop. Transgenic plants offer a viable alternative to decreasing reliance on synthetic pesticides, owing to their superior ability to resist pests and enhance crop yield. The primary advantages of these plants lie in their reduced environmental impact, achieved via the decreased need for pesticide application, lower carbon dioxide emissions, reduced production costs, and the production of relatively healthier products about pesticide usage. However, it is important to acknowledge the potential drawbacks of transgenic plants, including the risk of allergies, potential toxicity concerns, and consumer acceptance. Additionally, the potential development of resistance over time poses a significant weakness [55]. To mitigate these weaknesses, a recommended approach is the integration of relatively safe biological pesticides with other pest management strategies, thereby minimizing the limitations associated with transgenic plants. In recent years, there have been reports regarding the presence of resistance alleles in Lepidoptera species, particularly Helicoverpa, towards resistant plants. It has been observed that transgenic Bt cotton varieties have not been entirely effective in managing this pest. Consequently, the use of specific plant extracts has gained significant attention as they demonstrate the ability to induce mortality in these pests, as well as reduce their reproduction and feeding activities [56]. Commercially available products based on plant extracts have been introduced for the control of cotton pests, such as Sero-X®, which incorporates the active extract derived from Clitoria ternatea L. (Fabaceae). This particular product has been introduced as a means to combat Helicoverpa sp. and sucking pests of cotton [56]. In one study, the effectiveness of extracts from three plants, including tobacco (Nicotiana tabacium), neem (Azadirachtin indica), and datura (Datura stramonium), in controlling the cotton-pink bollworm (Pectinophora gossypiella), was investigated. The results showed that spraying tobacco plant extract directly on the leaves had the greatest impact on reducing the pest population, followed by neem and datura extracts. The study revealed that these plant extracts remained highly effective for approximately 48 h, but their effectiveness diminished thereafter, highlighting the need for frequent application. Additionally, the extracts were found to be environmentally friendly towards natural predators of pests, making them a promising option for pest management [57]. A study was conducted to explore the effectiveness of plant-based pesticides, including A. indica, Khaya senegalensis, and Hyptis suavuolens, both individually and in combination with half the recommended dose of synthetic pesticides, against the cotton bollworm. The findings demonstrated that using the full, recommended dose of synthetic pesticides or combining them with neem seed extract (at a rate of 6 kg/ha) was the most successful approach for controlling the cotton bollworm. Moreover, the use of plant extracts was found to be more cost effective. Importantly, the study highlighted that the application of plant extracts did not have any negative effects on natural predators of pests [58]. When considering the application of plant extracts, specifically aqueous extract or oil as field pesticides, the following studies are worth noting. Through the conducted investigations on pest control methods for Bt cotton plants in the field, it was discovered that plant extracts exhibited a considerably lower impact on the activity of natural predators of cotton pests when compared to synthetic insecticides [59]. In a study carried out in sub-Saharan Africa, it was determined that a total of 37 plant species extracts are utilized for the management of cotton pests in agricultural fields. The most prominent among these species include A. indica, Cassia nigricans, Ocimum gratissimum, Cymbopogon citratus, and Citrus sp., as well as Anacardium occidentale and Hyptis suaveolens. The findings of this investigation strongly suggest that the oil extracts derived from these plants possess significant potential in substituting synthetic pesticides [60]. The aforementioned studies provide evidence of the efficacy of these compounds as biopesticides, particularly in terms of their compatibility with natural enemies, which represents a significant advantage. Conversely, their limited persistence in natural environments, while posing a weakness in terms of increased spraying frequency, also contributes to their environmental benefits. These compounds tend to lose their effectiveness due to exposure to sunlight and can be easily washed away by rainwater. To overcome these challenges, the adoption of novel technologies, such as various branches of nanotechnology, including the production of nanoparticles or the nanoencapsulation of materials, can enhance the durability of these biopesticides. Considering the environmentally friendly nature of these materials, integrating them with other pest management approaches can serve as a viable alternative to synthetic insecticides. Biopesticides, which encompass bacteria, fungi, viruses, plant extracts, nematodes, and other biological agents, are not exclusively derived from natural sources. However, their effectiveness is enhanced via the incorporation of preservatives, carriers, and companions, which prevent their degradation and depletion in the environment. These formulations must possess characteristics such as affordability, environmental friendliness, minimal risk to natural enemies, and efficacy at the intended site of action. By combining biopesticides with other management strategies, integrated pest management can be effectively employed to suppress pest populations below economically damaging levels while minimizing adverse effects on non-target organisms and preserving ecosystem integrity [61].
Future research directions in the field of plant extract-based pesticides should focus on investigating the stability of plant extract inhibitors under field conditions and assessing their safety to non-target organisms. Specifically, studies should evaluate the stability of bioactive compounds in plant extracts under varying environmental conditions and determine the degradation rates of plant extract inhibitors in different formulations. Additionally, toxicity studies should be conducted to assess the impact of plant extract inhibitors on beneficial insects and other non-target organisms, while investigating the sub-lethal effects and potential interactions with beneficial organisms. Furthermore, the application of nanotechnology in this field should be explored to enhance the efficacy and delivery of plant extract inhibitors. Investigations into the development of nanoformulations, such as nanoemulsions or nanocapsules, can improve the stability and controlled release of plant extracts. Additionally, the potential of nanomaterials as carriers for plant extract compounds should be explored to enhance their efficacy and targeted delivery to pests. Furthermore, it is crucial to assess the safety and environmental impact of nanomaterial-based formulations on non-target organisms for sustainable pest management strategies. By integrating nanotechnology into plant extract-based pesticides, we can unlock new possibilities for effective and environmentally friendly crop protection solutions.

5. Conclusions

The current investigation showed that extracts from Leguminosae (sophora, bean, and pea) and Gramineae (wheat, barley, and corn) seeds considerably reduced Helicoverpa armigera’s digestive alpha-amylase activity. With inhibition rates of 95.26%, 94.65%, and 94.73%, respectively, the 0–30% fractions of wheat, barley, and sophora exhibited the strongest inhibitory activity. A range of 8–10 was the ideal pH range for inhibition. According to these results, extracts from seeds belonging to the Gramineae and Leguminosae families may be employed as biopesticides to manage H. armigera. In order to produce extracts with even higher inhibitory activity and to assess the safety and effectiveness of these extracts under field circumstances, more research is required to optimize the extraction and fractionation processes. Biopesticides can be made more effective in a variety of ways with the application of nanotechnology. To encapsulate and distribute biopesticides to certain locations, like the insect’s gut, for instance, nanoparticles can be utilized. This may enhance the biopesticides’ absorption by insects and shield them against deterioration.

Author Contributions

Conceptualization, M.C., T.O., L.B., R.F.P. and N.A.; methodology, N.A.; software, M.C., R.F.P. and N.A.; validation, M.C., N.A., L.B., R.F.P. and T.O.; formal analysis, M.C., R.F.P. and N.A.; investigation, M.C. and N.A.; resources, M.C., A.C.B. and N.A.; data curation, M.C.; writing—original draft preparation, M.C. and N.A.; writing—review and editing, M.C., L.B., T.O., R.F.P. and A.C.B.; visualization, T.O., L.B., M.C., N.A. and A.C.B.; supervision, M.C., L.B. and T.O.; project administration, M.C. and L.B.; funding acquisition, T.O. and L.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

Sima Panahirad from the University of Tabriz’s Department of Horticulture revised the manuscript, and her insightful suggestions greatly enhanced it. She edited and reviewed the work. The authors truly thank and respect her.

Conflicts of Interest

The authors declare no conflicts of interest.

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Sustainability 16 00145 g001
Figure 1. The inhibitory effect of the several seed extracts (wheat, barley, sophora, corn, bean, and pea) on alpha-amylase activity in H. armigera. (Different letters indicate significant statistical differences between treatments).
Figure 1. The inhibitory effect of the several seed extracts (wheat, barley, sophora, corn, bean, and pea) on alpha-amylase activity in H. armigera. (Different letters indicate significant statistical differences between treatments).
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Figure 2. Inhibition of plant (sophora, wheat, barley, corn, bean, and pea) extracts’ different fractions on the H. armigera alpha-amylase enzyme. Similar letters in each row show the lack of a significant difference at the 1% probability level.
Figure 2. Inhibition of plant (sophora, wheat, barley, corn, bean, and pea) extracts’ different fractions on the H. armigera alpha-amylase enzyme. Similar letters in each row show the lack of a significant difference at the 1% probability level.
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Figure 3. Comparison of the alpha-amylase enzyme inhibition percentage in Helicoverpa armigera via seed extracts’ application at different pH values.
Figure 3. Comparison of the alpha-amylase enzyme inhibition percentage in Helicoverpa armigera via seed extracts’ application at different pH values.
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Table 1. Ammonium Sulfate Salt Quantities for Various Concentrations.
Table 1. Ammonium Sulfate Salt Quantities for Various Concentrations.
Concentration RangeQuantity of Ammonium Sulfate Salt (grams)
0–30%1.7
30–50%1.2
50–70%1.29
70–80%0.67
Table 2. Variance Analysis of the inhibitory impact of wheat, barley, sophora, corn, pea, and bean on the activity of alpha-amylase in H. armigera.
Table 2. Variance Analysis of the inhibitory impact of wheat, barley, sophora, corn, pea, and bean on the activity of alpha-amylase in H. armigera.
Change SourceFreedom DegreeSquare AveragesF
Inhibition value5917.55920.237 **
Error1245.340
Total17
** Significant difference at the 1% probability level.
Table 3. Mean analysis of the inhibitory effect of some plant extract fractions on H. armigera alpha-amylase.
Table 3. Mean analysis of the inhibitory effect of some plant extract fractions on H. armigera alpha-amylase.
PlantChange SourceFreedom DegreeSquare AveragesF
WheatTreatment33932.930303.185 **
Error812.972
BarleyTreatment33443.646841.724 **
Error84.091
CornTreatment33257.333324.680 **
Error81.032
SophoraTreatment33731.633661.298 **
Error85.643
BeanTreatment31450.98524.508 **
Error859.205
PeaTreatment3147.95378.741 **
Error8
** Significant difference at the 1% probability level.
Table 4. The comparison of the inhibition average percentage of different plant seed extract fractions on the alpha-amylase activity in H. armigera. Similar letters in each row show the lack of a significant difference at the 1% probability level. (Different letters indicate significant statistical differences between treatments).
Table 4. The comparison of the inhibition average percentage of different plant seed extract fractions on the alpha-amylase activity in H. armigera. Similar letters in each row show the lack of a significant difference at the 1% probability level. (Different letters indicate significant statistical differences between treatments).
Fraction 0–30%30–50%50–70%70–80%
Plant
Wheat95.26 a73.42 b24.44 c21.02 c
Barley94.65 a82.92 b42.89 c19.34 d
Corn83.62 a41.31 b16.85 c11.22 c
Sophora94.73 a54.25 b15.08 c15.58 c
Bean52.71 a13.43 b8.23 b5.95 b
Pea50.76 a26.25 b8.72 c2.50 c
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Chamani, M.; Askari, N.; Pourabad, R.F.; Bouket, A.C.; Oszako, T.; Belbahri, L. Potential Biopesticides from Seed Extracts: A Sustainable Way to Protect Cotton Crops from Bollworm Damage. Sustainability 2024, 16, 145. https://doi.org/10.3390/su16010145

AMA Style

Chamani M, Askari N, Pourabad RF, Bouket AC, Oszako T, Belbahri L. Potential Biopesticides from Seed Extracts: A Sustainable Way to Protect Cotton Crops from Bollworm Damage. Sustainability. 2024; 16(1):145. https://doi.org/10.3390/su16010145

Chicago/Turabian Style

Chamani, Masoud, Narjes Askari, Reza Farshbaf Pourabad, Ali Chenari Bouket, Tomasz Oszako, and Lassaad Belbahri. 2024. "Potential Biopesticides from Seed Extracts: A Sustainable Way to Protect Cotton Crops from Bollworm Damage" Sustainability 16, no. 1: 145. https://doi.org/10.3390/su16010145

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