Buffalo-bur (Solanum rostratum Dunal) invasiveness, bioactivities, and utilization: a review

Review methodology

Our comprehensive review involved an exhaustive search across various reputable scientific platforms and journal databases to gather a diverse array of research papers. The primary sources included Web of Science, Wiley Online Library, Cambridge University Press, ScienceDirect, PubMed Centre, Google Scholar, and ACS Publications. Among these, the Web of Science emerged as the predominant platform, contributing significantly to the wealth of literature examined. To optimize our search strategy, we strategically employed a range of keywords, including “Solanum”, “S. rostratum”, “S. rostratum + distribution”, “S. rostratum + invasive”, “S. rostratum + purification”, and “S. rostratum + phytochemistry”. These keywords were meticulously chosen to encompass diverse aspects of our research objectives, ensuring a comprehensive exploration of the literature landscape related to S. rostratum. Subsequently, the identified papers underwent a rigorous selection process, with only the most relevant and germane studies being included and cited in our analysis. This meticulous curation aimed to uphold the quality and precision of our review, aligning with the specific focus and objectives of our research.

Phytochemical constituents present in s. rostratum

Alkaloids

Alkaloids represent a diverse group of secondary chemical compounds widely present in plants, recognized as a defense mechanism against insects, microorganisms, animals, and humans due to their structural variety. In S. rostratum, the main alkaloids (Fig. 4) include pyrrole alkaloids, methylprotodioscin, phenylethylamine, solanine, chaconine, and glycosidic alkaloids (Novruzov, Aslanov & Ismailov, 1973; Bah et al., 2004; Zhang et al., 2012; Liu et al., 2019; Liu et al., 2021). Pyrrole alkaloids are a class of naturally occurring compounds that contain a five-membered ring composed of four carbon atoms and one nitrogen atom found in various plants, fungi, and marine organisms where it serves as a chemical defense against predators and protection against environmental stresses (Singh & Majik, 2019). Liu et al. (2021) recently identified and isolated three pairs of novel enantiomeric pyrrole alkaloids—(2′ R)-Caffeicpyrrole A and (2′ S)-Caffeicpyrrole A, (2′ R)-Caffeicpyrrole B, and (2′ S)-Caffeicpyrrole B, and (2′ R)-Caffeicpyrrole C and (2′ S)-Caffeicpyrrole C—from the leaves of S. rostratum where it confirms its efficacy as an antifeedant and growth-inhibitory agent against Henosepilachna vigintioctomaculata, an invasive herbivore of S. rostratum.

Furthermore, other studies indicated that phenylethylamine, extracted from the aerial parts of S. rostratum, displayed anti-feedant activity against Helicoverpa armigera (Liu et al., 2019). Also, methylprotodioscin, isolated from the aerial parts of S. rostratum, demonstrated its capability to induce cytotoxic effects on human cancer cells (Bah et al., 2004). In another study, solanine and chaconine were isolated and identified from various parts of S. rostratum, demonstrating their potential in controlling pests, especially those with chewing and sucking mouthparts on a variety of vegetable crops (Zhang et al., 2012).

Flavonoids

S. rostratum, classified in the Androceras section series, is recognized for its abundance of flavonoids (Huang et al., 2017). Important flavonoids have been isolated and identified from S. rostratum (Fig. 5). Quercetin is one of the major flavonoids primarily sourced from the aerial part of S. rostratum that plays a crucial role in neutralizing free radicals in the body, promotes seed germination and plant development in both stressful and non-stressful environments (Huang et al., 2017; Omar et al., 2018). As a plant-derived aglycone, quercetin has demonstrated superior disease-fighting abilities compared to curcumin, exhibiting higher reduction potential, a 3.5-fold increase in total antioxidant capacity, and a reduction in reactive oxygen species (ROS) and nitric oxide (NO) in LPS-stimulated human THP-1 acute monocytic leukemia cells (Zhang et al., 2011). Additionally, quercetin mitigates mycotoxin-induced endoplasmic reticulum stress and apoptosis, providing cellular protection (Yang et al., 2020). Another aglycone flavonoid, kaempferol, has been successfully isolated from S. rostratum (Ibarra-Alvarado et al., 2010; Huang et al., 2017). Kaempferol demonstrates potential in treating obesity-related ailments by promoting lipolysis and suppressing adipogenesis in 3T3-L1 adipocytes, a mouse pre-adipocyte cell line (Muni Swamy et al., 2020). It has also been reported to inhibit the growth of pancreatic cancer cells through apoptosis induction (Zhang et al., 2008). Hesperitin, another major flavonoid found in S. rostratum (Ibarra-Alvarado et al., 2010) has been associated with reducing cancer cell proliferation by inducing cell cycle arrest and exhibiting cytostatic effects (De Oliveira, Santos & Fernandes, 2019). Likewise, luteolin, a flavonoid in S. rostratum (Wang et al., 2015) has been linked to inhibiting tumor growth by influencing cellular processes such as apoptosis, angiogenesis, migration, and cell cycle progression (Çetinkaya & Baran, 2023) as well as suppressing some proinflammatory mediators such as IL-6, IL-8, TNF-α, and COX-2 which in turn regulates different skin inflammatory processes (Gendrisch et al., 2021).

Other compounds

The phenolic constituents in S. rostratum contributes to its potential economic significance where the total phenols identified in S. rostratum (Valadez Vega et al., 2019) have been reported to have the ability to mitigate oxidative stress (Phuyal et al., 2020), function as food preservatives (Derakhshan et al., 2018), and exhibit substantial significance (p < 0.05) in the treatment of callus using elicitors (Ali, El-Nour & Yagi, 2018). Terpene glycosides are non-volatile natural products responsible for a number of bioactivities in plants (Schwab, Fischer & Wüst, 2015). Linalyl-β-glucopyranoside, a terpene glycoside, was found to be present in the chloroform extract from the aerial part of S. rostratum after analysis with the Folin–Ciocalteu reagent (Omar et al., 2018). Linalyl-β-glucopyranoside also referred to as linalool glucoside, functions as an aroma precursor subsequent to the release of linalool (Moon et al., 1994). The chemical structure of linalyl-β-glucopyranoside is illustrated in Fig. 6.

Furthermore, a diverse array of phytochemicals present in S. rostratum contributing to distinct bioactivities have been compiled in Table 2.

Biological activities associated with S. rostratum

Anti-inflammatory activity

S. rostratum, has been recognized for its profound anti-inflammatory activity, making it a compelling subject of study in the realm of natural medicine. The plant’s anti-inflammatory effects can be attributed to its rich phytochemical composition, including alkaloids, flavonoids, and phenolic compounds. These bioactive constituents have demonstrated the ability to modulate key inflammatory pathways and mediators. Studies have revealed that S. rostratum extracts possess inhibitory effects on pro-inflammatory cytokines, such as tumor necrosis factor-alpha (TNF-α) and interleukin-6 (IL-6), crucial players in the inflammatory response. Moreover, the plant’s extracts have been found to downregulate the activity of enzymes like cyclooxygenase-2 (COX-2) and inducible nitric oxide synthase (iNOS), further attenuating inflammatory processes. This anti-inflammatory potential positions S. rostratum as a valuable resource for traditional medicine and suggests its potential application in the development of anti-inflammatory drugs. The elucidation of the specific mechanisms underlying its anti-inflammatory activity holds promise for the advancement of therapeutic interventions targeting inflammatory disorders. In humans, sitosteryl glucosides have demonstrated in vivo anti-inflammatory activity on important pro-inflammatory enzymes such as cyclooxygenases (COX-1 and COX-2 (ovine/human)) and lipoxygenases (human recombinant-5-LOX enzyme) that are mediators for a number of inflammations and sensitized diseases observed in the body (El-Feky & El-Rashedy, 2023). Additionally, methylprotodioscin, found in S. rostratum, has been reported for its application in treating chronic intestinal inflammation by ameliorating intestinal mucosal inflammation through the regulation of intestinal immunity, thereby enhancing the differentiation of the intestinal barrier (Zhang et al., 2015).

In animals, the sitosteryl glucosides compound isolated from S. rostratum has also been recognized for its anti-inflammatory properties, particularly in combating Tissue-type Plasminogen Activator (TPA)-induced mouse ear edema (Alvarez et al., 2009) as well as Carrageenan induced paw edema (Naikwadi, Phatangare & Mane, 2022).

Anti-carcinogenic activity

S. rostratum, has exhibited noteworthy anti-carcinogenic activities, marking it as a promising candidate in cancer research. Extensive studies have uncovered bioactive compounds within S. rostratum that contribute to its anti-carcinogenic properties. Alkaloids, flavonoids, and phenols found in this plant have demonstrated inhibitory effects on cancer cell proliferation and metastasis. These compounds, through various molecular mechanisms, showcase potential in suppressing the growth of cancer cells, inducing apoptosis, and impeding angiogenesis. Additionally, the richness of phytochemical composition present in S. rostratum has shown promise in mitigating oxidative stress, a factor implicated in cancer development. The plant’s anti-inflammatory properties further contribute to its anti-carcinogenic potential, as chronic inflammation is closely linked to cancer progression. The exploration of anti-carcinogenic activities of S. rostratum not only underscores its significance in traditional medicine but also presents an avenue for the development of novel therapeutic interventions in the field of oncology. Further research is warranted to elucidate specific molecular pathways involved and optimize the utilization of S. rostratum in potential anti-cancer treatments. Due to the abundant phenolic content found in S. rostratum, the ethyl acetate extract from this plant has been noted for its ability to exhibit anti-carcinogenic activity against human malignant cell lines, particularly those associated with breast adenocarcinoma and cervix squamous cancer. This was substantiated by a significant decrease in cell viability (Valadez Vega et al., 2019). Additionally, the aerial portion of S. rostratum is employed in the preparation of infusions, that helps regulate vaginal fluids, disinfect genital areas, and serve as a supplementary element in the treatment of uterine cancer.

Antifungal and antimicrobial activity

In Mexico, the hydroalcoholic extract of S. rostratum has also been noted for its ability to impede the growth of key fungi (isolates 501 and 498 of Candida albicans, isolates 434 and 514 of Aspergillus fumigatus, isolates 1526 and 1591 of Histoplasma capsulatum, and isolates 168 and 167 of Coccidioides immitis) associated with pulmonary mycoses, a fungal disease characterized by lung tissue necrosis and the development of vascular thrombosis (Alanís-Garza et al., 2007).

Additionally, S. rostratum exhibits antifungal activity against Curvularia lunata, a causal fungus of corn leaf spot disease, where it causes a significant growth inhibition (inhibition by 80%) when exposed to the extract of this plant (Hernandez-Rodriguez et al., 2018).

Herbicidal/phytotoxic activity

S. rostratum demonstrates considerable potential in controlling common weeds that can adversely impact the growth of economically important plants. Extracts from various parts of S. rostratum have been found to inhibit the seed germination and development of several common weeds like Poa annua, Amaranthus retroflexus, and a common vegetable, Solanum lycopersicum (Ping, Zhu & Zhang, 2012; Shao, 2015; Zhou et al., 2021). The soil surrounding S. rostratum harbors various fungi, including Aspergillus flavus, which exhibits allelopathic behavior toward Amaranthus retroflexus, Thlaspi arvense, and Poa annua by producing the mycotoxin, kojic acid, that affects the normal functioning of these plants (Shao et al., 2017). Furthermore, essential oils extracted from S. rostratum have demonstrated efficacy in inhibiting the growth and development of Amaranthus retroflexus, impacting shoot and root length growth as well as seed germination. S. rostratum also exerts phytotoxic effects on Arabidopsis thaliana, a model organism, by inhibiting root elongation and seed germination (Liu et al., 2023). Additionally, secondary metabolites such as thymine, adenosine, and cerevisterol, isolated from an endophytic fungus Purpureocillium sp. found in S. rostratum, have been reported to exhibit inhibitory activity against the growth of Amaranthus retroflexus, through the inhibition of seed sprouting and a reduction in root length (Kuchkarova et al., 2020).

Insecticidal and pesticidal activities

S. rostratum has demonstrated growth-inhibitory effects against Helicoverpa armigera, a pest that primarily feeds on Fabaceae, Malvaceae, Poaceae, and Solanaceae plants (Cunningham & Zalucki, 2014), where it has also shown to cause an inhibition in the feeding process of this pest thus positioning it as a viable pesticide (Liu et al., 2019). Here, the ethyl acetate fraction demonstrated the best anti-feedant activity by 80% against Helicoverpa armigera at the highest concentration (0.5 mg/mL), outperforming water and petroleum ether fractions (Liu et al., 2019). In a similar investigation, S. rostratum displayed antifeedant and growth-inhibitory activity against Henosepilachna vigintioctomaculata through the isolation of three pairs of novel enantiomeric pyrrole alkaloids its leaves. The results revealed enantioselectivity with all enantiomers demonstrating both antifeedant and growth-inhibitory activities having the R configuration at C-2′ exhibiting the most potent effects (Liu et al., 2021). Last but not the least, the extracts of S. rostratum have been utilized as insecticides to control lepidopterous larvae and aphids on fruit and vegetable crops due to their high toxicity, repellent properties, anti-feeding effects, and stomach poisoning effects, thereby mitigating the impact of these insects on crops and reducing economic losses (Zhang et al., 2012).