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2023 Volume 3
Article Contents
Abstract
Introduction
Perennial grasses as natural allies of soil health
Perennial grasses as natural allies of soil biodiversity
Perennial grasses in climate change mitigation
Perennial grasses in combating invasive plants
Conclusions
Author contributions
Data availability
Acknowledgments
Conflict of interest
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References
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ARTICLE   Open Access    

Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats

  • Department of Biochemistry, Federal University of Technology, Akure 340252, Nigeria

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  • Vegetables are vital for balanced diets as they are a good source of nutraceuticals for humans. This study looks to assess the underlying preventive mechanisms of wild lettuce (WL) and African eggplant leaves (AE) in hypertensive rats. The experimental rats were grouped into seven groups with six rats in each group as follows: Normotensive rats (group 1); hypertensive (HYP) rats (group 2); HYP rats treated with captopril (10 mg/kg/day) (group 3); HYP rats treated with WL (250 and 500 mg/kg/day) (group 4 and 5 respectively) and HYP rats treated EP (250 and 500 mg/kg/day) (group 6 and 7). The experiment lasted for 14 d. Administration of WL and EP leaves extract normalized altered activity of angiotensin 1 converting enzymes (ACE), arginase, and acetylcholinesterase (AChE) in treated HYP rats when compared with the untreated HYP rats. Also, nitric oxide (NO) levels and antioxidant status were enhanced in the treated HYP rats when compared with the untreated HYP rats. Meanwhile, some of the antihypertensive preventive mechanisms of WL and EP leaves were able to modulate the altered activity of ACE, arginase, AChE, enhanced endothelial function (improved NO production and reduced arginase activity), and improved antioxidant prowess when compared with untreated HYP rats. Remarkably, WL leaves had better anti-hypertensive properties than EP leaves. Nevertheless, the consumption of these vegetables could be a veritable dietary approach to actualizing healthy status in a hypertensive state.

  • Introduction

    Perennial grasses [e.g., switchgrass (Panicum virgatum), big bluestem (Andropogon gerardii), indiangrass (Sorghastrum nutans), little bluestem (Schizachyrium scoparium), Maasai love grass (Eragrostis superba), and bush ryegrass (Enteropogon macrostachyus)] are plant species that live for more than two years with deep root systems and the capacity to grow in a variety of climates[1−5]. Although often overlooked, perennial grasses serve an important role in ecosystems, particularly in maintaining soil health and biodiversity, climate change mitigation, and combating alien invasive plants (AIPs)[1,4]. Thus, they are simply natural allies for soil biodiversity conservation, invasive plant management, and climate change mitigation[6,7]. The deep root systems of perennial grasses help soil structure by improving aeration, increasing water infiltration, and lowering soil erosion[1,5]. Also, their extensive root network supports the stability of the soil, making it less susceptible to degradation and encouraging a healthier ecology overall[1,8]. Further, they play a key role in the nutrient cycle by maximizing nutrient utilization and minimizing leaching[9,10]. In addition, perennial grasses contribute organic matter to the soil through biomass, which decomposes over time and enriches the soil with critical nutrients[11−13]. This process improves soil fertility, increasing productivity for other plant species, and agricultural activities[9,12].

    IAPs, also known as non–native or exotic species, are plants introduced to an ecosystem where they do not naturally occur[14−16] and pose a severe ecological, economic, and social impacts[17,18]. Unlike native species, IAPs often lack natural enemies and diseases in their new environments, allowing them to proliferate unrestrictedly[19,20]. Their invasions lead to the displacement of native flora as they outcompete native species for resources i.e., light, water, and nutrients[21,22]. As a result, causing a reduction in biodiversity and the alteration of ecosystem functions, often forming dense monocultures that hinder the growth of other plants and disrupt habitats for native wildlife[23,24]. Moreover, IAPs can alter soil chemistry and hydrology thereby negatively impacting soil biodiversity[6,7,15,25]. IAPs can further impact human health by increasing allergens and providing a habitat for disease vectors[15]. Efforts to manage IAPs typically involve early detection, prevention, and rapid response, such as biological control, mechanical removal, and herbicide treatment[19,25,26]. Although the role of perennial grasses in combating IAPs has been seldom investigated, available studies show that effective management requires integrated eco-friendly management incorporating competitive native perennial grasses to suppress IAPs[6,8,15,27].

    Furthermore, perennial grasses are ecologically significant because they enhance species diversity and soil biodiversity i.e., living forms found in soil, which includes microorganisms (bacteria and fungi), mesofauna (nematodes and mites), and macrofauna, i.e., earthworms and insects[28−32]. This diversity is critical to ecosystem function and plays an important role in nutrient cycling, soil structure maintenance, and plant growth promotion[29,30]. They contribute to nutrient-cycling activities by breaking down organic materials into simpler compounds that perennial grasses and other plants can consume, decomposing dead plants and animals, and releasing nutrients back into the soil, thus increasing soil fertility[32−34]. Further, perennial grasses also promote plant-soil symbiotic relationships such as mycorrhizal associations and rhizobium symbioses, which improves soil health and plant growth[29]. These benefits are enhanced by perennial grasses' root exudates, which support both soil microbial diversity and activity, resulting in a more dynamic and resilient soil environment[1]. However, extreme weather events, such as floods and droughts, as well as IAPs can cause soil organism loss and structural damage, thereby impeding the roles of soil organisms[35−37]. Further, increased temperatures can disrupt microbial activity and nitrogen cycling mechanisms, impacting soil health, and productivity[37,38]. Addressing these challenges needs long-term integrated management approaches that maintain natural ecosystems and increase soil biodiversity, as well as IAP control and climate change mitigation. For instance, promoting the use and maintaining the diversity of perennial grasses in rangelands and agricultural habitats[1,39,40].

    Climate change which is the average change in the earth's temperature and precipitation patterns can also disrupt the delicate balance of soil biodiversity[37,41]. It is driven primarily by human activities i.e., burning fossil fuels, deforestation, and industrial processes which lead to an unprecedented rise in greenhouse gases, such as carbon dioxide and methane in the atmosphere[37,42]. Often the earth's surface temperature increases concomitantly with these greenhouse gasses[41]. Increased temperatures contribute to sea-level rise, more frequent and intense heatwaves, wildfires, and droughts affecting biodiversity, water supply, and human health. Changes in precipitation patterns also lead to extreme weather events i.e., hurricanes, floods, and heavy rainfall, disrupting ecosystems and human societies[37]. It also negatively impacts biodiversity, as species must adapt, migrate, or face extinction due to altered habitats and shifting climate zones[36]. Addressing climate change requires global cooperation and robust policies aimed at reducing greenhouse gas emissions which include the use of eco-friendly approach, for instance, keeping the environment intact with native plants i.e., perennials grasses[43]. Perennial grasses (e.g., turfgrass) are considered potential for mitigating the effects of climate change because they have a high carbon sequestration capacity, storing carbon in both soil and aboveground biomass[44−46]. They can contribute to reducing greenhouse gas levels by absorbing and storing carbon dioxide from the atmosphere in their roots and tissues, thus helping to mitigate climate change[44]. Furthermore, their capacity to minimize greenhouse gas emissions through reduced tillage and increased nitrogen use efficiency makes them an important component of habitat restoration to mitigate climate change impacts[43].

    Consequently, native perennial grasses have been recommended by various previous studies to be used for habitat restoration, including rangelands, because of their physiological and morphological traits, which have shown great potential to improve soil health and biodiversity, mitigate climate change, and combat IAPs[1,5,8,27,40,47]. By their competitive and morphological traits, several perennial native grass species found in African rangelands (e.g., African foxtail grass (Cenchrus ciliaris), horsetail grass (Chloris roxburghiana), rhodes grass (Chloris gayana), E. superba, and E. macrostachyus) and P. virgatum, S. nutans, S. scoparium, and A. gerardii in North America have been tested and recommended for ecological restoration[1−5].

    Perennial grasses as natural allies of soil health

    Preceding studies have demonstrated that perennial grasses have the potential to improve soil health and structure in rangelands and protected habitats[1,48−50]. Unlike annual plants, which have shallow root systems, perennial grasses can penetrate deep into the soil, sometimes reaching depths of several meters as they have deep and extensive root systems[1,7,40]. These deep roots create channels that enhance soil aeration, allowing for better oxygen flow and water infiltration, thereby preventing soil compaction[49]. Perennial grasses contribute to soil stability by binding soil particles together, thereby preventing erosion (Fig. 1), which is important in ecosystems or habitats prone to heavy rainfall or wind[48,49]. This stabilization effect reduces the loss of topsoil, which contains the highest concentration of organic matter and nutrients essential for plant growth[44]. Moreover, perennial grasses have been reported to be efficient in nutrient cycling, a critical process for maintaining soil fertility[49]. For instance, their deep roots access nutrients in deeper soil layers, which might be unavailable to shallow-rooted plants[49,50]. These nutrients are then brought to the surface and incorporated into the plant biomass. When the grasses die back or shed leaves, these nutrients are returned to the soil surface as organic matter, making them accessible to other plants[32,49,51]

    Figure 1.  Diagram illustrating the multifaceted benefits of perennial grasses and their interconnected roles in promoting soil health, biodiversity, IAPs control, climate change mitigation, water retention, erosion control, and habitat provision. The arrows illustrate the complex interactions and synergies among these components, emphasizing the comprehensive ecological contributions of perennial grasses. The central position of perennial grasses highlights their pivotal role in these areas. This visual representation emphasizes how perennial grasses contribute to and enhance various aspects of ecosystem health and stability.
    DownLoad: Full-Size Img PowerPoint

    Furthermore, perennial grasses enhance soil health and structure (Fig. 1), improving the soil's ability to retain water and withstand extreme weather events i.e., heavy rainfall and floods[44,49]. Their extensive root networks stabilize the soil, reducing erosion and runoff (Fig. 1), which are critical for maintaining soil fertility and agricultural productivity under variable climatic conditions[51]. The continuous growth and decay cycle of perennial grasses contributes to the slow but steady release of nutrients[52]. This slow release is beneficial for maintaining a stable nutrient supply, as opposed to the rapid nutrient depletion often seen in soils dominated by annual crops[50]. This process also helps in reducing nutrient leaching, where nutrients are washed away from the soil profile, particularly nitrogen, which is critical for plant growth[49]. Perennial grasses help to reduce N2O emissions; excess nutrients can lead to increased N2O emissions[10,11,53]. They also contribute significantly to the soil organic matter, which is a key component of soil health[52]. Organic matter consists of decomposed plant and animal residues, which improve soil structure, water retention, and nutrient availability[50,52]. The biomass produced by perennial grasses, both above and below ground, adds a substantial amount of organic material to the soil[52]. As the plant material decomposes, it forms humus, a stable form of organic matter that enhances soil structure by increasing its capacity to hold water and nutrients[52,54]. This is particularly important in dry regions e.g. in Africa, where water retention can be a limiting factor for crop growth[49]. The organic matter also provides a habitat and food source for a diverse array of soil organisms, including bacteria, fungi, and earthworms, which further contribute to soil fertility through their biological activities[43,52,54].

    Perennial grasses as natural allies of soil biodiversity

    Perennial grasses play a crucial role in enhancing soil biodiversity (abundance and diversity) and activities within the soil[31,32,51,54]. They provide critical habitats for soil fauna i.e., earthworms, nematodes, and arthropods (Fig. 1)[32,54]. Their complex root systems create a stable environment that supports a wide range of soil organisms[55]. Also, the root systems of perennial grasses exude a variety of organic compounds, including sugars, amino acids, and organic acids, which serve as food sources for soil biodiversity[54]. This continuous supply of root exudates and a stable environment fosters a diverse macro and microbial community, which is essential for maintaining soil health[31,43,54]. For instance, it was reported by Smith et al.[54] that in areas with abundant perennial grasses, a high soil macrofaunal biodiversity (i.e., Lumbricidae, Isopoda, and Staphylinidae) was observed. They further asserted that these grasses were beneficial to soil macrofauna as they increased the abundance and species diversity of staphylinid beetles, woodlice, and earthworms. In addition, Mathieu et al.[56] reported the influence of spatial patterns of perennial grasses on the abundance and diversity of soil macrofauna in Amazonian pastures. These findings suggest that well-managed perennial grasses are vital in enhancing soil macro and microbes in ecosystems[54−56].

    These soil organisms perform various functions, including decomposing organic matter, fixing atmospheric nitrogen, and suppressing soil-borne diseases[29,30,32]. A diverse soil macro and microbial community can enhance nutrient cycling, making nutrients more available to plants[30,56]. Enhanced microbial diversity by perennial grasses contributes to the suppression of pathogens through competition and the production of antimicrobial compounds, thus promoting plant health[32]. They also help in maintaining soil structure, fertility, and overall ecosystem function[32]. For instance, earthworms, often referred to as 'ecosystem engineers', augment soil structure by creating burrows that improve aeration and water infiltration in perennial grass communities[31,51]. Their activity also helps mix organic matter into the soil, promoting nutrient cycling[31,32]. Nematodes and arthropods which feed on perennial grass species contribute to the decomposition process, breaking down organic matter and releasing nutrients that are vital for plant growth[31,54]. The presence of a diverse soil fauna community is indicative of a healthy soil ecosystem, which is more resilient to environmental stresses and disturbances[31].

    Furthermore, perennial grasses are considered as being instrumental in promoting plant-soil symbiotic relationships[43,54], which are crucial for plant health and soil fertility. One of the most well-known symbiotic relationships is between plants and mycorrhizal fungi[29,33]. These fungi colonize plant roots and extend their hyphae into the soil, increasing the root surface area and enhancing the plant's ability to absorb water and nutrients, particularly phosphorus. The relationship between perennial grasses and mycorrhizal fungi is mutually beneficial. The fungi receive carbohydrates produced by the plant through photosynthesis, while the plant gains improved access to soil nutrients and increased resistance to soil-borne pathogens[30]. This symbiotic relationship is particularly important in nutrient-poor soils, where mycorrhizal associations can significantly enhance plant growth and survival. Additionally, perennial grasses promote other beneficial plant-soil interactions, such as those involving nitrogen-fixing bacteria. These bacteria form nodules on the roots of certain perennial grasses, converting atmospheric nitrogen into a form that plants can use[29,30]. This process is essential for maintaining soil fertility, especially in ecosystems where nitrogen is a limiting nutrient.

    Perennial grasses in climate change mitigation

    Perennial grasses are increasingly recognized for their role in climate change mitigation (Fig. 1)[43,44,57]. They can sequester carbon, reduce greenhouse gas emissions, and adaptation to climate variability[58,59]. Their deep root systems and grass-like characteristics make them highly effective in capturing and storing carbon[44]. These roots can penetrate deep into the soil and store carbon for extended periods[59]. Because of this, perennial grasses show potential to enhance the resilience of ecosystems to changing climatic conditions[44]. The roots of perennial grasses are more extensive and persistent compared to annual crops, allowing for greater carbon storage both in the root biomass and the soil[45,46,60]. This process of carbon sequestration involves capturing atmospheric carbon dioxide (CO2) through photosynthesis and storing it in perennial grass tissues (e.g., turfgrasses) and soil organic matter[44−46]. Preceding studies have further shown that perennial grasses can sequester substantial amounts of carbon, contributing to the reduction of atmospheric CO2 levels[45,61]. In addition to carbon sequestration, perennial grasses can reduce greenhouse gas emissions through various mechanisms[43]. One of the primary ways is by reducing the need for frequent soil tillage, which is common in annual cropping systems. Tillage disrupts soil structure, releases stored carbon as CO2, and increases soil erosion[58,61]. Thus, with their long lifespan, perennial grasses can reduce the need for tillage, thereby minimizing CO2 emissions from soil disturbance[43,58].

    Moreover, perennial grasses can improve nitrogen use efficiency, reducing the need for synthetic fertilizers that are a major source of nitrous oxide (N2O) emissions—a potent greenhouse gas[53,62]. Their deep root systems enable them to access nutrients from deeper soil layers, reducing nutrient leaching and the subsequent emissions of N2O[53]. By optimizing nutrient use, perennial grasses contribute to lower greenhouse gas emissions associated with agricultural practices[63]. Also, perennial grasses are crucial for adapting to climate variability[44]. Their deep root systems allow them to access water from deeper soil layers, making them more resilient to drought conditions compared to annual crops[44]. This water use efficiency helps maintain plant growth and productivity even during periods of water scarcity, which are expected to become more frequent with climate change[49]. In general, perennial grasses support soil biodiversity conservation through habitat provision, climate change mitigation, and promoting ecosystem resilience[58]. Besides, these grasses are crucial for ecosystem stability and productivity, particularly in the face of climate change, and ensure the continued provision of ecosystem services (Fig. 1).

    Perennial grasses in combating invasive plants

    Previous studies have shown that IAPs pose significant threats to ecosystems worldwide by displacing native species, altering habitats, and disrupting ecosystem functions and services[15,20,23,64]. Among the integrated management techniques to combat IAPs involves the use of competitive native plants (Fig. 1) such as perennial grasses[6,7,40]. These grasses, which live for more than two years with robust root systems, growth, and resilience to varying environmental conditions, offer several advantages in controlling IAPs[1,48]. Their competitive growth patterns and ability to restore and maintain native plant communities, and establish, and thrive in diverse habitats make them formidable competitors against invasive plants[1]. One of the primary ways perennial grasses combat IAPs is through competition for resources[48]. Their extensive root systems allow them to efficiently absorb water and nutrients, outcompeting IAPs that typically have shallower roots. This competitive edge limits the resources available to IAPs, inhibiting their growth and spread. For instance, species like P. virgatum and big A. gerardii are known for their deep roots, which can reach depths of up to 10 feet (3 m), providing them with a significant advantage over many IAPs[8,48]. They can also outcompete IAPs through their competitive growth patterns including quick establishment and forming dense canopies that shade out AIPs[1,8]. For example, native perennial grasses like S. nutans and S. scoparium have been shown to effectively compete with invasive species i.e., spotted knapweed (Centaurea stoebe) by limiting light availability and space for growth[8,48].

    Moreover, using their extensive root systems that stabilize the soil, perennial grasses can prevent erosion and invasions of IAPs[44]. Invasive plants i.e., carrot weed (Parthenium hysterophorus), cheatgrass (Bromus tectorum), and kudzu (Pueraria montana) can rapidly colonize disturbed soils, leading to severe erosion problems[20,65,66]. However, perennial grasses i.e., P. virgatum and big A. gerardii have been found to reduce erosion and creating an unfavorable environment for IAPs to establish owing to their deep fibrous root systems that hold the soil in place. Perennial grasses can also modify the microenvironment in ways that make it less conducive for IAPs[1,27,66]. They produce dense root mats that strengthen the organic matter content and soil structure, improving the fertility and health of the soil. The diversity and growth of native plant species is aided by improved soil conditions, which further promote biodiversity and inhibit IAPs by strengthening ecosystem resilience[48].

    Additionally, the use of perennial grasses in restoration has shown promising results in reclaiming areas overrun by IAPs and maintaining native plant communities that are disrupted by IAPs[8,66]. By planting a mix of native perennial grasses, land managers can restore ecological balance and prevent the re-establishment of IAPs[26]. These grasses provide long-term ground cover and habitat for wildlife, contributing to the overall health and stability of the ecosystem[1,8,54]. By reintroducing native perennial grasses into areas (e.g., rangelands and protected habitats) dominated by IAPs, ecosystems, and their biodiversity can be restored to their earlier conditions[27,39,67]. For instance, the use of native perennial grasses has been successful in restoring prairie ecosystems that were previously overrun by IAPs i.e., leafy spurge (Euphorbia esula) and purple loosestrife (Lythrum salicaria)[68]. Another important example of using perennial grasses to mitigate IAPs is the restoration of tallgrass prairies in the Midwest United States[8,66]. These prairies were historically dominated by native perennial grasses i.e., S. nutans and S. scoparium, however IAPs i.e., smooth brome (Bromus inermis) and reed canarygrass (Phalaris arundinacea) displaced them, leading to biodiversity loss and altered ecosystem functions[8,66,68]. Studies show that following the restoration of these invaded habitats using perennial grasses, native grasses successfully reestablished and reduced IAPs and promoting native biodiversity[66,67]. In addition, another notable example is the use of perennial grasses to restore riparian areas which were heavily invaded and impacted by IAPs i.e., giant reed (Arundo donax) and saltcedar (Tamarix spp.)[67,69]. Planting native perennial grasses like western wheatgrass (Pascopyrum smithii) and creeping wildrye (Elymus triticoides) in these areas helped to stabilize the soil, reduce erosion, and suppress IAPs, leading to improved riparian habitat quality and ecosystem resilience[18,66,67,69].

    Therefore, competitive suppressive perennial grasses are a crucial tool in the fight against IAPs and other weeds. Their competitive abilities, contributions to soil health, and role in ecosystem restoration makes them invaluable in managing and alleviating the impacts of IAPs. As research continues, the potential for perennial grasses to be integrated into broader IAP strategies remain significant, promising a more sustainable and ecologically sound approach to preserving native biodiversity.

    Conclusions

    Perennial grasses are pivotal in enhancing soil biodiversity, mitigating climate change, and combating IAPs. Their deep root systems stabilize soils, support diverse soil faunal communities, and improve water retention. Besides, they are important grasses in sequestering carbon, reducing greenhouse gas emissions, suppressing IAPs, and supporting the reestablishment of native plant communities. Integrating perennial grasses into protected areas and rangelands management practices could offer a sustainable solution to pressing environmental challenges including invasions of IAPs. Stakeholders i.e., farmers, conservationists, ecologists, and land managers are advised to use perennial grass systems in their restoration practices, crop rotations, and pasturelands to enhance soil health and resilience. They are further commended to use perennial grasses for erosion control and to improve soil structure and fertility. Policymakers could develop and support policies that incentivize the use of perennial grasses in agricultural and restoration projects. Researchers, they are advised to conduct studies to quantify the long-term benefits of perennial grasses on soil biodiversity and climate change mitigation. Additionally, they can develop country or region-specific guidelines for the effective use of perennial grasses in different ecosystems. Hence, by integrating perennial grasses into our environmental stewardship strategies, we can ensure a thriving, balanced ecosystem capable of withstanding the impacts of climate change and IAPs.

    Author contributions

    The author confirms sole responsibility for the following: review conception and design, and manuscript preparation.

    Data availability

    Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

    Acknowledgments

    The author thanks all the colleagues who reviewed and proofread this article. This work was not supported by any funding agency.

  • The author declares that there is no conflict of interest.

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  • Cite this article

    Agunloye OM, Olawuyi EA, Oboh G. 2023. Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats. Food Materials Research 3:7 doi: 10.48130/FMR-2023-0007
    Agunloye OM, Olawuyi EA, Oboh G. 2023. Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats. Food Materials Research 3:7 doi: 10.48130/FMR-2023-0007
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Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats

  • Department of Biochemistry, Federal University of Technology, Akure 340252, Nigeria

  • Received: 13 January 2023
  • Accepted: 24 March 2023
  • Published online: 31 May 2023
Food Materials Research  3,  Article number: 7  (2023)  |  Cite this article

Abstract: Vegetables are vital for balanced diets as they are a good source of nutraceuticals for humans. This study looks to assess the underlying preventive mechanisms of wild lettuce (WL) and African eggplant leaves (AE) in hypertensive rats. The experimental rats were grouped into seven groups with six rats in each group as follows: Normotensive rats (group 1); hypertensive (HYP) rats (group 2); HYP rats treated with captopril (10 mg/kg/day) (group 3); HYP rats treated with WL (250 and 500 mg/kg/day) (group 4 and 5 respectively) and HYP rats treated EP (250 and 500 mg/kg/day) (group 6 and 7). The experiment lasted for 14 d. Administration of WL and EP leaves extract normalized altered activity of angiotensin 1 converting enzymes (ACE), arginase, and acetylcholinesterase (AChE) in treated HYP rats when compared with the untreated HYP rats. Also, nitric oxide (NO) levels and antioxidant status were enhanced in the treated HYP rats when compared with the untreated HYP rats. Meanwhile, some of the antihypertensive preventive mechanisms of WL and EP leaves were able to modulate the altered activity of ACE, arginase, AChE, enhanced endothelial function (improved NO production and reduced arginase activity), and improved antioxidant prowess when compared with untreated HYP rats. Remarkably, WL leaves had better anti-hypertensive properties than EP leaves. Nevertheless, the consumption of these vegetables could be a veritable dietary approach to actualizing healthy status in a hypertensive state.

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    Introduction

    • Hypertension is one of the major cardiovascular diseases and it has become a major menace to public health. The worldwide index has shown that more than one-quarter of the world population has hypertension[1]. Hypertension and its accompanying complications can cause morbidity and mortality[2]. Interestingly, hypertension is a multifactorial pathology that involves alteration in the activity of the renin-angiotensin-aldosterone system (RAAS)[3], cholinesterase[4], arginase[5], inflammation[6], chronic inflammation causes oxidative stress[7] and endothelial dysfunction[8]. Also, oxidative stress plays a significant role in the manifestation of hypertension by causing the endothelial system to malfunction, thereby impairing nitric oxide production and its vasodilation process[9]. In general practice, hypertension is managed through the use of antihypertensive medications which often cause side effects such as coughing, erection problems and sleep issues[10].

      Nowadays, natural products have been used as a frontline alternative therapeutic agent for the management of hypertension. This may have been a result of their availability as well as little or no side effects following use. Remarkably, medicinal foods have become a popular alternative source of therapy for the management of various health-related issues, and have a proven scientific basis to support their folklore claims. However, vegetables which form a greater proportion of the human daily diet, have been referred to as protective foods because they are endowed with diverse bioactive compounds which offer varying health benefits such as modulation of immunity, prevention of gastrointestinal disorders, cardiovascular diseases, cancer, diabetes, and other chronic diseases. In Africa, a lot of vegetables are used as part of daily meals, not because of their nutritional properties or edibility only but because most of these vegetables provide health-enhanced benefits[11].

      African wild lettuce (Launaea taraxacifolia) is an annual West Tropical Africa herb commonly known as wild lettuce. Wild lettuce is among some of the vegetables that are on the verge of extinction. Wild lettuce is wide spread in some African countries such as Nigeria, Ghana and Sierra Leone. Wild lettuce leaves are commonly consumed as soup, salad or eaten as spinach[12]. A number of research studies have indicated that wild lettuce leafs have antioxidant properties[13], protective effects against DNA and kidney damage[14] antimicrobial and antiarthritic effects[15] and hypolipidaemic properties[14, 15]. Also, a study has shown that wild lettuce leaf has been used for the management of liver diseases, dyslipidemia, and diabetes[13, 14]. In the same vein, wild lettuce leaf has a diverse amount of macro and micronutrients which make it a good choice of vegetable for healthy living.

      African eggplant (Solanum macrocarpon), also known as efo igbagba in southwestern Nigeria is a local leafy vegetable that is cultivated mainly for its leaves. Unlike the other solanum varieties, its bitter taste has made the fruits less edible[16]. Macrocarpon has many benefits. It is readily available, cheap, and nutritious and it can be used to prepare soup. Kaushik et al.[17] maintained that Solanum macrocarpon could be used to treat tuberculosis, convulsion and boost infertility and insomnia in women in the traditional way. The leaves can be boiled to extract the juice which can be used to alleviate jaundice, asthma and whooping cough[18]. Also, infusion from Solanum macrocarpon leaves have been used for the treatment of some ailments such as of some diseases such as liver disease, dyslipidemia, and diabetes[19,20]. However, as reported in folk medicine, these vegetables exhibit cardioprotective properties with a dearth of information on their underlying mechanisms through which acclaimed health benefits could be achieved. Therefore, the present study sought to unravel the underlying mechanism through which wild lettuce and African eggplant leaves exhibit antihypertensive properties in L-NAME-induced hypertensive rats.

    Materials and methods

      Sample collection and preparation

    • The African wild lettuce leaves (Launaea taraxacifolia) and African eggplant leaves (Solanum macrocarpa L.) were obtained from a farm settlement in Akure, Ondo state, Nigeria. The vegetables were authenticated by Mr Momoh, a Forest Biologist at the herbarium, Federal University of Technology, Akure (FUTA), Nigeria. Then, the leafy part was removed, rinsed, air-dried, pulverized and sieved into powdery form. The aqueous extract was prepared by dispersing 500 mg of each sample in 250 mL of distilled water and vigorously shaking for 24 h using a HY-4 speed governing multipurpose oscillator (HINOTEK, Ningbo, China). The mixture was initially filtered using a sieving mesh while subsequent filtration was carried out with Whatman filter paper and the obtained filtrate was lyophilized to obtain a powdered form of the samples.

      Chemicals and reagents

    • Chemicals such as N(ω)-nitro-L-arginine methyl ester (L-NAME), Hippuryl-L-Histidyl-L-Leucine (HHL), thiobarbituric acid (TBA) and other chemicals and reagents used for this study were of analytical grade, while all-glass distillers used for water distillation were of high grade

      Experimental grouping and protocol

    • Healthy male Wistar strain rats (number = 10, weight: 180–200 g, age 11–12 weeks) were sourced from the University of Ibadan (Nigeria). Thereafter, the institution's research committee granted ethical clearance for the utilization of experimental rats. The National and Institutional guidelines for animal protection and welfare were followed strictly. The rats were maintained at room temperature (25 °C) with free access to food and water. They were allowed to adapt to their new environment for 2 weeks prior to the commencement of induction and treatment. Thereafter, acclimatized rats were administered with 40 mg/kg body weight (BW) except for group 1 rats and the treatment regime lasted for 14 d. Experimental rats were fed with animal feed with six rats per group.

      Experimental design

    • Group I: Normotensive;

      Group II: Hypertensive (HYP) rats;

      Group III: HYP rats administered with captopril [10 mg/kg body weight (BW)];

      Group IV: HYP rats administered with 250 mg/kg BW of wild lettuce;

      Group V: HYP rats administered with 500 mg/kg BW of wild lettuce;

      Group VI: HYP rats administered with 250 mg/kg BW of African eggplant;

      Group VII: HYP rats administered with 500 mg/kg BW of African eggplant daily

      Thereafter, the experimental rats were sacrificed, tissues of interest were collected, homogenized and the homogenate was used for biochemical evaluations.

    Biochemical assays

      Determination of ACE activity

    • The heart and kidney ACE activity was determined as described by Cushman & Cheung[21]. The substrate [hippuryl-histidylleucine (Bz-Hip-HisLeu)] was purchased from Sigma Aldrich. The amount of cleaved hippuric acid from hippuric-histidyl-leucine was measured by the enzymatic method. Sample (50 μL) and 150 μL of 8.33 mM of hippuric-histidyl-leucine (Bz-Hip-His-Leu) in 125 mM Tris-HCl buffer (pH 8.3) were incubated at 37 °C for 30 min. After incubation, the reaction was arrested by adding 250 μL of 1 M HCl. The Gly–His bond was then cleaved, and the hippuric acid produced by the reaction was extracted with 1.5 mL ethyl acetate. Next, the mixture was centrifuged to separate the ethyl acetate layer; then, 1 mL of the ethyl acetate layer was transferred to a clean test tube and evaporated. The residue was redissolved in distilled water, and its absorbance was measured at 228 nm. The plasma ACE activity was expressed as μmol HHL cleaved/min

      Determination of arginase activity

    • Arginase activity in the heart and kidney tissue was determined by measuring the rate of urea production using α-isonitrosopropriophenone (9% in absolute ethanol) as previously described by Kaysen & Strecker[22]. Briefly, 50 μl of samples were added into 75 μl of Tris-HCl (50 mmol/l, pH 7.5) containing 10 mmol/l MnCl2 and was pre-incubated at 37 °C for 10 min to activate the enzyme. The hydrolysis reaction of L-arginine by arginase was performed by incubating the mixture containing activated arginase with 50 μl of L-arginine (0.5 mol/l, pH 9.7) at 37 °C for 1 h and was stopped by adding 400 μl of the acid solution mixture [H2SO4 : H3PO4 : H2O = 1:3:7 (v/v/v)]. For calorimetric determination of urea, α-isonitrosopropiophenone (25 μl, 9% in absolute ethanol) was then added and the mixture was heated at 100 °C for 45 min. After placing the sample in the dark for 10 min at room temperature, the urea concentration was determined spectrophotometrically by the absorbance at 550 nm. The amount of urea produced was used as an index for arginase activity. The arginase activity was expressed as μmol urea produced/min/mg protein.

      Determination of acetylcholinesterase activity

    • The AChE enzymatic assay was determined according to the method of Ellman et al.[23]. The reaction mixture (2 ml final volume) contained 100 mM K+-phosphate buffer, pH 7.5 and 1 mM 5,5′-dithiobisnitrobenzoic acid (DTNB). The method is based on the formation of the yellow anion, 5,5′-dithio-bis-acid-nitrobenzoic, measured by absorbance at 412 nm during 2 min incubation at 25 °C. The enzyme (40–50 mg of protein) was pre- incubated for 2 min. The reaction was initiated by adding 0.8 mM acetylthiocholine iodide (AcSCh) for acetylcholineterase assay. All samples were in triplicate readings and the enzyme activities were expressed in units/mg of protein.

      Nitric oxide level (NOx) determination

    • NOx content was estimated in a medium containing 70 μl of the sample, 70 μl of 2% vanadium chloride (VCl3) in 5% HCl, 70 μl of 0.1% N-(l-naphthyl) ethylenediamine dihydrochloride and 2% sulphanilamide (in 5% HCl) in 1:1 ratio. After incubating at 37 °C for 60 min, nitrite levels, which correspond to an estimative level of NOx, were determined spectrophotometrically at 540 nm, based on the reduction of nitrate to nitrite by VCl3[24]. The nitrite and nitrate levels were expressed as nanomoles of NOx/mg protein.

      Estimation of the total thiol level

    • The total thiol level was determined in the tissue (heart, kidney and lung) and homogenates according to the method previously described by Ellman[25]. The reaction system was made up of 170 mL of 0.1 M potassium phosphate buffer (pH 7.4), 20 mL of sample, and 10 mL of 10 mM DTNB. At the end of 30 min incubation at room temperature, the absorbance was measured at 412 nm. A standard curve was plotted for each measurement using reduced glutathione (GSH) as a standard and the results were expressed as mmol/mg protein.

      Determination of tissue lipid peroxidation

    • The lipid peroxidation assay was carried out using the modified method of Ohkawa et al.[26]. Briefly, 300 μl of tissue (plasma, heart, kidney and lungs) homogenate, 300 μl of 8.1% SDS (Sodium dodecyl sulphate), 500 μl of Acetic acid/HCl (PH = 3.4) and TBA (Thiobarbituric acid) were added, and the mixture was incubated at 100 °C for 1 h. Thereafter, the thiobarbituric acid reactive species (TBARS) produced was measured at 532 nm and calculated as Malondialdehyde (MDA) equivalent.

      Total protein determination

    • Protein was measured by the Coomassie blue method according to Bradford[27] using serum albumin as standard.

      Data analysis

    • The values were expressed as mean ± standard deviation (SD). The mean differences in each group were analyzed by one-way ANOVA using Graph pad prism 5.0, followed by a posthoc test using Turkey s multiple range tests at the level p < 0.05.

      Results

    • Figure 1 represents the heart and kidney ACE activity of normotensive rats, untreated hypertensive, and treated hypertensive rats. The result as presented showed that hypertensive rats had higher activity of ACE when compared with the normotensive rats. However, administration of captopril (20 mg/kg BW), wild lettuce (WL) and African eggplant leaf (AP) (250 and 500 mg/kg BW) respectively caused a reduction in the ACE activity when compared with the untreated hypertensive rats. Comparatively, WL administration had less activity ACE in hypertensive rats than AP.

      Figure 1. 

      Effect of wild lettuce and African eggplant leaves extract on (a) lungs and (b) kidney ACE activity in L-NAME induced hypertension in rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive (p < 0.05).

      Also, Fig. 2 depicts the heart and kidney arginase activity of arginase of normotensive, hypertensive and treated hypertensive rats. Obtained results revealed an elevated arginase activity in the hypertensive rats when compared with normotensive rats. Thereafter, administration of captopril (20 mg/kg BW), WL and AP leaf extract (250 and 500 mg/kg BW) brings about a reduction in arginase activity in the treated hypertensive rats in comparison with the hypertensive rats.

      Figure 2. 

      Effect of wild lettuce and Africa eggplant leaves extract on the (a) heart and (b) kidney arginase activity in L-NAME induced hypertension in rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive (p < 0.05).

      Furthermore, Fig. 3 depicts the activity of AChE in the heart and kidney of normotensive and untreated and treated hypertensive rats. As obtainable, untreated hypertensive rats had significantly (p < 0.05) higher AChE activity when compared with the normotensive rats. Meanwhile, administration of captopril, WL and AP leaf extract (250 and 500 mg/kg body weight respectively) caused the elevated AChE activity to be minimal in the treated hypertensive rats when correlated with untreated hypertensive rats.

      Figure 3. 

      Effect of wild lettuce and Africa eggplant leaves extract on the (a) heart and (b) kidney acetylcholinesterase (AChE) activity in L-NAME induced hypertension in rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive (p < 0.05).

      Likewise, Fig. 4 depicts the level of nitric oxide (NO) in normotensive rats and hypertensive (untreated and treated). Interestingly obtained results showed that hypertensive rats had a declining level of NO in the plasma, heart, kidney and lungs when compared with the NO level of normotensive rats. Meanwhile, the plasma, heart, kidney and lungs NO level of treated hypertensive rats was observed higher with respect to what is obtainable for the untreated hypertensive rats. Nevertheless, WL-treated groups had higher NO levels than AP-treated groups.

      Figure 4. 

      Effect of wild lettuce and Africa eggplant leaves extract on (a) plasma, (b) heart, (c) kidney and (d) lungs Nitric oxide level in L-NAME induced hypertension in rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract treated hypertensive with hypertensive (p < 0.05).

      Furthermore, heart, kidney and lung total thiol levels as presented in Fig. 5. As presented, untreated hypertensive rats exhibited reduced levels of total thiol in comparison with normotensive rats. Remarkably, hypertensive rats treated with captopril, WL and AP aqueous extract (250 and 500 mg/kg BW respectively) exhibited higher total thiol levels when compared to the untreated hypertensive rats. Comparatively, WL and AP at 500 mg/kg body weight enhanced total thiol levels significantly higher than 250 mg/kg body weight.

      Figure 5. 

      Effect of wild lettuce and Africa eggplant leaves extract on the (a) heart, (b) kidney and (c) lungs total thiol level in L-NAME induced hypertension in rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive (p < 0.05). β Not significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive.

      Also, Fig. 6 represents TBARS levels in the plasma, heart, kidney and lungs of experimental rats. As presented, normotensive and treated hypertensive rats had lower TBARS levels in plasma, heart, kidney and lung in comparison with untreated hypertensive rats.

      Figure 6. 

      Effect of wild lettuce and African eggplant leaves extract on malondialdehyde level in (a) plasma, (b) heart, (c) kidney and (d) lungs of L-NAME induced hypertensive rats. Values represent mean ± standard deviation (n = 6). * Significantly different when compared normotensive with hypertensive (p < 0.05). ** Significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive (p < 0.05). β Not significantly different when compared wild lettuce and African eggplant leaves extract-treated hypertensive with hypertensive.

      Finally, Fig. 7 and Table 1 show the peaks on the chromatogram and corresponding bioactive compound constituents of wild lettuce (WL) and African eggplant (AP) leaves obtained using GC-MS analysis. As shown on the chromatogram, 12 bioactive compounds listed as follows: P-coumaric acid, cinnamic acid, Quercetin, Syringic acid, Kaempferol and others were quantified from wild lettuce and African eggplant leaves respectively as shown in Table 1.

      Figure 7. 

      (a) GC-MS fingerprint of wild lettuce (Launaea Taraxacifolia) leaves bioactive constituents. (b) GC-MS fingerprint of African eggplant (Solanum macrocarpon) leaves bioactive constituents.

      Table 1.  Bioactive compound constituent of wild lettuce and African eggplant leaves.

      S/NCompounds detectedMolecular formulaPhenolic content (mg/g)
      Wild
      lettuce      		African eggplant
      11,2,3-BenzenetriolC6H6O30.040.02
      2Gentisic acidC5H11NO20.030.02
      3Benzoic acid, 4-hydroxy-C7H6O30.360.38
      4Cinnamic acidC12H16O2Si1.221.31
      5Syringic acidC15H26O5Si21.071.03
      6Protocathecolic acidC16H30O4Si30.320.49
      7KaempferolC27H44O6Si40.910.62
      8QuercetinC15H10O71.181.14
      93-Caffeoyl quinic acidC34H66O9Si60.410.54
      10CathecolC12H22O2Si20.440.54
      11TyrosolC14H26O2Si20.010.02
      12P-coumaric acidC9H8O31.311.41
    Discussion

    • Vegetables constitute a critical portion of the human diet. WL and EP have been used by Nigerian local dwellers for the management of some diseases such as hypertension without scientific basis. Experimentally, administration of L-NAME at 40 mg/kg BW causes a hypertensive effect in normotensive rats[28,29] as well as a manifestation of oxidative stress[30]. Hypertension is a multifactorial pathology which involves alteration in the activity of some enzymes like ACE, arginase, cholinergic and purinergic enzymes as well as oxidative stress[31]. It is worth noting that one of the mechanisms through which L-NAME causes hypertension is via ACE up-regulation[32]. As presented (Fig. 1), the elevated ACE activity was drastically reduced after the administration of WL and AP aqueous extract to the L-NAME-induced hypertensive rats. It should be on a note that ACE causes hypertension via its catalytic effect on angiotensin I which result in the formation of angiotensin II, a potent vasoconstrictor[32]. In addition to the production of angiotensin II, ACE also enhanced the degradation of the potent vasodilator, bradykinin which eventually contribute to the hypertensive effect of ACE activity[33]. The WL and EP leaf extracts administrated caused a sharp decline in the activity of ACE in the hypertensive rats serving as an indicator for the anti-hypertensive protective mechanism of the selected vegetable. Likewise, the availability of bradykinin will be enhanced by reduced ACE activity since this will ensure the vascular-promoting effect of bradykinin[34]. This observed inhibition or reduction in the activity of ACE could be linked to the effect of diverse bioactive compounds in the WL and EP leaves. Studies have shown that hydroxyl, carboxylic, sulfurhydric or o-methylation groups of the plant bioactive compounds interact with Zinc II ion residues at the active site of the ACE protein which might cause an alteration in the active site resulting in the observed reduction in activity[35]. Research findings have shown that the dietary approach offers a protective effect against hypertensive effects[36,37]. Also, findings from this study agree with previous reports on the effect of bioactive compounds from vegetables on ACE activity[38,39].

      Arginase play a prominent function in the development of hypertension via its negative direct effect on NO-level production. L-NAME administration significantly impairs NO production[40] via its inhibitory effect on endothelial nitric oxide synthase (eNOS). eNOS and arginase compete for available L-arginine for their respective bioactivity. In a hypertensive state, elevated arginase activity has been observed which implies that the majority of the available L-arginine will be utilized by arginase and this implies that the NO production by e-NOS will be impaired[41]. It should be noted that elevated arginase activity in hypertensive individuals and in rats’ models has been reported as high[34]. As presented, WL and EP leaves extract lower arginase activity in L-NAME-induced hypertensive rats, implying that L-arginine will be preserved for e-NOS for NO production.

      The observed high NO level is possible due to a reduction in the enzymatic activity of arginase, thereby ensuring more NO availability for the vasodilatory processes. However, administration of aqueous extract reversed the L-NAME inhibitory effect on e-NOS, reduced the activity of arginase and ensure an ample amount of NO for vasodilatory processes. The observed effect on arginase activity and NO level further explained another antihypertensive mechanism of wild lettuce and African eggplant leaves[42,43]. Also, research findings have shown that AChE contributes to the onset of cardiovascular diseases such as hypertension. Elevated AChE activity causes a significant reduction in acetylcholine bioavailability causing constriction of smooth muscle[31]. The eNOS mediated smooth muscle vasodilation and relaxation role in conjunction with released acetylcholine (ACh) from the cholinergic nerves as reported by Kellogg Jr et al.[44]. ACh availability is subjected to the hydrolytic effect of AChE which hydrolyzes ACh to Acetate and choline[45]. The WL and EP leaves ability to reduce the activity of AChE in hypertensive rats could be a result of their phytochemical constituents as presented in Fig. 7 and Table 1.

      Oxidative stress has been implicated in the development of hypertension justified by the presence of a well-established mechanism of cellular injury known as lipid peroxidation[46]. Also, administration of an aqueous extract of WL and EP leaves significantly enhanced the endogenous antioxidant status of the hypertensive rats as grossly considered by an enhanced level of total thiol level with a corresponding decrease in TBARS level in the treated hypertensive rats. The result of our study showed that L-LAME administration has the ability to promote oxidative imbalance adjudged by lipid peroxidation and drastically reduce the level of total thiol in the untreated experimental rats, the antioxidant defence mechanism potential of WL and EP leaves against oxidative stress was reflected in their ability to minimise TBARS level and elevate the level of total thiol in treated rats. This implies that the bioactive constituent of WL and EP leaves could prevent the rapid depletion of the antioxidant capacity of hypertensive rats. Vegetables have been reported to exhibit diverse antioxidant properties due to the presence of polyphenolic compounds[46,47].

      In conclusion, this study has revealed some underlying mechanisms through which WL and EP leaves exhibits anti-hypertensive effect. Wild lettuce and African eggplant leaves reduced ACE, arginase and AChE activity and enhanced NO levels in hypertensive rats. Also, the occurrence of bioactive compounds such as P-coumaric acid, cinnamic acid, quercetin, syringic acid, Kaempferol and others may have responsible for the anti-hypertensive property and antioxidant effect. However, WL showed more antihypertensive potential compared to EP leaves, nonetheless, both vegetables have the ability to ameliorate hypertensive effects. Therefore, the vegetables selected for this study should be prevented from going into extinction.

    Compliance with ethical standards

    • The institution and Department of Animal Ethics Committee approved the use of experimental animals prior to the commencement of the study.

      Conflict of interest

      • The authors declare that they have no conflict of interest.

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      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Nanjing Agricultural University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (7)  Table (1) References (47)
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    Agunloye OM, Olawuyi EA, Oboh G. 2023. Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats. Food Materials Research 3:7 doi: 10.48130/FMR-2023-0007
    Agunloye OM, Olawuyi EA, Oboh G. 2023. Modulatory effect of wild lettuce and African eggplant leaf extract on key enzymatic activity linked to hypertension in L-NAME induced hypertensive rats. Food Materials Research 3:7 doi: 10.48130/FMR-2023-0007
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  • Introduction
  • Materials and methods

  • Sample collection and preparation

  • Chemicals and reagents

  • Experimental grouping and protocol

  • Experimental design

  • Biochemical assays

  • Determination of ACE activity

  • Determination of arginase activity

  • Determination of acetylcholinesterase activity

  • Nitric oxide level (NOx) determination

  • Estimation of the total thiol level

  • Determination of tissue lipid peroxidation

  • Total protein determination

  • Data analysis

  • Results

  • Discussion
  • Compliance with ethical standards
  • Conflict of interest
  • Rights and permissions
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