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Botanical Sciences

versión On-line ISSN 2007-4476versión impresa ISSN 2007-4298

Bot. sci vol.100 no.4 México oct./dic. 2022  Epub 01-Ago-2022

https://doi.org/10.17129/botsci.3004 

Review

Phytochemical composition and biological activities of the plants of the genus Randia

Composición fitoquímica y actividades biológicas de las plantas del género Randia

Manrique Ojeda-Ayala1 
http://orcid.org/0000-0002-9050-3669

Soila Maribel Gaxiola-Camacho1 
http://orcid.org/0000-0002-5078-7636

Francisco Delgado-Vargas2  3  * 
http://orcid.org/0000-0003-3369-5200

1Laboratorio de Parasitología, Doctorado en Ciencias Agrícolas, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Sinaloa (UAS), Culiacán, Sinaloa, México.

2Unidad de Investigaciones en Salud Pública “Dra. Kaethe Willms”, Facultad de Ciencias Químico-Biológicas, UAS, Ciudad Universitaria, Culiacán, Sinaloa, México.

3 Laboratorio de Química de Productos Naturales, Posgrado en Ciencia y Tecnología de Alimentos, Facultad de Ciencias Químico-Biológicas, UAS, Ciudad Universitaria, Culiacán, Sinaloa, México.


Abstract

Background:

The genus Randia L. (Rubiaceae) is native to Americas and highly distributed in tropical areas. Some Randia species are used in traditional medicine in some countries to treat diverse illnesses/symptoms of kidney, circulatory system, lungs, diabetes, cancer, inflammation, and against the bites/stings of snakes and other poisonous animals.

Questions:

What are the phytochemical compounds previously identified in Randia? What biological activities do they present?

Data description:

Twenty-eight studies on chemical composition and biological activities of Randia were reviewed. Species names were corroborated in Plants of the World Online and World Flora Online.

The site and studied years:

Studies of Randia of Americas from 1991 to 2021.

Methods:

Database reviewed were PubMed, Scopus, Scielo, BVS, DAOJ, Science Direct, Springer Link, Web of Science, and Google Scholar, employing the keywords Randia and its synonym Basanacantha.

Results:

Six species are the most studied (R. aculeata, R. echinocarpa, R. ferox, R. hebecarpa, R. matudae, and R. monantha). Ethnopharmacology information of 12 species was recovered. One hundred compounds in Randia have been identified (phenolic acids, terpenes, sterols, and others), and diverse biological activities reported in 24 studies (e.g., antimutagenic, antioxidant, and antivenom) have demonstrated for nine species.

Conclusions:

Biological activities found in some species of Randia support their traditional uses, but only the antivenom effect of Randia aculeata has been demonstrated. Randia species could be a source of bioactive compounds; however, knowledge must be expanded to demonstrate their traditional uses and contribute to the development of strategies for their preservation and rational use.

Keywords: Bioactive compounds; ethnopharmacology; herbal medicine; natural compounds; Rubiaceae

Resumen

Antecedentes:

El género Randia L. (Rubiaceae) es originario de América y está altamente distribuido en zonas tropicales. Algunas de sus especies son utilizadas en la medicina tradicional de algunos países para tratar diversos padecimientos/síntomas: renales, circulatorios, pulmonares, diabetes, cáncer, inflamación y contra las mordeduras/picaduras de serpientes y animales ponzoñosos.

Preguntas:

¿Cuáles son los compuestos fitoquímicos identificados en Randia? ¿Qué actividades biológicas presentan?

Descripción de datos:

Se revisaron 28 estudios sobre composición química y actividades biológicas de Randia. La nomenclatura se corroboró en Plants of the World Online y World Flora Online.

Sitio y años de estudio:

Estudios de Randia de América desde 1991 a 2021.

Métodos:

Las bases de datos revisadas fueron PubMed, Scopus, Scielo, BVS, DAOJ, Science Direct, Springer Link, Web of Science y Google académico, empleando las palabras clave Randia y su sinónimo Basanacantha.

Resultados:

Seis especies de Randia son las más estudiadas (R. aculeata, R. echinocarpa, R. ferox, R. hebecarpa, R. matudae y R. monantha). Se recuperó información etnofarmacológica de 12 especies. Cien compuestos han sido identificados en Randia (ácidos fenólicos, terpenos, esteroles y otros) y demostrado diversas actividades biológicas en 24 estudios (e.g., antimutagénica, antioxidante, antiveneno) para nueve especies.

Conclusiones:

Las actividades biológicas de especies de Randia soportan sus usos tradicionales, pero solo está demostrada la actividad antiveneno de R. aculeata. Especies de Randia podrían ser fuente de compuestos bioactivos, pero su conocimiento debe incrementarse para demonstrar sus usos tradicionales y contribuir al desarrollo de estrategias para su preservación y uso racional.

Palabras clave: Compuestos bioactivos; compuestos naturales; medicina herbolaria; etnofarmacología; Rubiaceae

The genus Randia L. is native to America, belongs to the Gardeniae tribe in the Rubiaceae family. The species of Randia are bushy, arboreal, or some lianas (POWO 2019). Three neotropical genera have been related to Randia: Basanacantha, Rosenbergiodendron, and Glossostipula (Hooker 1873, Gustafsson 1998, Lorence 1986). Randia and Basanacantha have been considered synonyms since 1919 (Stranczinger et al. 2007); whereas Rosenbergiodendron and Glossostipula are independent genera (Lorence 1986, 1999). The species of Randia grow in wooded areas at 0-3,300 m above sea level, in tropical and subtropical areas (Lorence 1986, Gustafsson 1998, 2000, Borhidi 2006). The morphological and molecular characterization of Randia spp. show the following characteristics: some are woody and dioecious, pollen in permanent tetrads, monolocular ovary with two parietal placentas, fruit with abundant seeds in a juicy pulp of black color, and short lateral branches with thorns in the knots. However, some exceptions include monoecious and hermaphrodite species (Lorence & Dwyer 1986, Burger & Taylor 1993, Gustafsson 2000). Analysis of the Gardeniae genera (i.e., vegetative, floral and fruit morphology, anatomy, and palynology) indicates that paleotropical species previously assigned to Randia belong to other genera (Keay 1958, Lorence & Nee 1987). The re-classified species are Randia dumetorum (Catunaregam spinosa (Thunb.) Tirveng.), Randia spinosa (Catunaregam spinosa (Thunb.) Tirveng.), Randia formosa (Rosenbergiodendron formosum (Jacq.) Fagerl.), Randia siamensis (Oxyceros horridus Lour.), Randia ruiziana (Rosenbergiodendron longiflorum (Ruiz & Pav.) Fagerl.), Randia tetrasperma (Himalrandia tetrasperma (Wall. ex Roxb.) T. Yamaz.), and Randia nilotica (Catunaregam nilotica (Stapf) Tirveng.) (POWO 2019, WFO 2021). Thus, Randia comprises 106 species distributed in Americas. Mexico is a center of diversity with 62 species (58.5 % of the total) and 44 of them are endemics (41.5 %) (Villaseñor 2016, POWO 2019, WFO 2021). Seven species have been identified since 2012 (Borhidi et al. 2013, Jiménez & Cruz 2013, Borhidi & Soto-Nuñez 2014, Borhidi & Salas-Morales 2014, Borhidi & Martínez-Salas 2015).

Traditional medicine includes the knowledge and practices based on theories, beliefs, and experiences of indigenous people of different cultures to maintain health and prevent/treat physical and mental diseases, including the traditional use of medicinal plants (OMS 2013). In traditional medicine, the used parts (leaves, stem, root, flower, or seed) depend on the plant, and its activity is associated with the content of secondary metabolites (Balandrin et al. 1993). Approximately 80 % of the world’s population employs traditional medicine, but most uses are not supported with scientific information (Vides & Alvares 2013). Mexico has a high floristic richness, and Mexican herbal traditional medicine includes a great diversity of phytotherapeutic treatments, including about 4,500 species, representing the second country with more registered medicinal plants globally (Barragán-Solís 2006).

People of different countries in America (e.g., Mexico, Colombia, Panama, and Brasil) use the leaves, stems, and fruit of several species of Randia in traditional medicine against a wide range of diseases (e.g., renal, respiratory, circulatory, cancer, malaria, snake bites) and symptoms (e.g., inflammation, pain, diarrhea) (Bye et al. 1991, Borhidi & Diego-Pérez 2008, Méndez-Valenzuela & Hernández-Martínez 2009, Erbano & Duarte 2011, Gallardo-Casas et al. 2012). In Mexico, ethnobotanical uses of Randia are known since 1,777 with records of Tarahumaras Indians that consumed the fruits of Randia echinocarpa Moc. & Sessé ex DC. and R. laevigata Standl., and scraps of the R. echinocarpa husks were used to prepare a sacramental maize beer (batari) (Irigoyen-Rascón & Paredes 2015). Besides, the early twentieth century reports indicate that R. echinocarpa preparations were used to treat diarrhea, malaria, and other kidney maladies (Martínez 1939). In this regard, most ethnopharmacological uses of the Randia species have not been scientifically demonstrated. However, biological activities of plants are due to their chemical constituents, so phytochemical characterization is essential. On this subject, the chemical studies of Randia are scarce despite the ethnobotanical importance of several of its species in America and particularly Mexico, where the genus is widely diversified. This review analyses the published information about ethnobotany, phytochemical characterization, and tested biological activities of Randia. The information presented here is useful to support future studies on developing supplemental foods or new phytotherapeutic agents.

Materials and methods

Systematic searches on the databases PubMed, Scopus, Scielo, Health Virtual Library (BVS), Directory of Open Access Journals (DOAJ), Science Direct, Springer Link, Web of Science, and Google Scholar were conducted, including dates from January 1940 to November 2021. The employed keywords were Randia and its synonym Basanacantha. The recovered information was classified accordingly to inclusion and exclusion criteria. Inclusion criteria: original papers, reviews, and books including information about ethnobotany, chemical characterization, and biological activities. Exclusion criteria: Original papers, reviews, theses, posters, and books on species originally classified as Randia but later reclassified into another genus.

A total of 6,914 results were discriminated as follows: first screening, 423 duplicates were removed; second screening, the titles of documents recovered were analyzed according to the selection criteria, and 6,344 results were eliminated; third screening, 30 results were removed by abstract reading; 147 full papers were reviewed, but 89 were excluded because the studied species were reclassified to other Rubiaceae genera (POWO 2019, WFO 2021). After discrimination, 28 original papers were recovered. Additionally, we included six books and two original papers not retrieved in the searches.

Results

Our review data included 30 original papers and six books with ethnobotanical, phytochemical, and biological activities studies for 15 of the Randia species, 14 % of the total richness of the genus (106 spp.). Scientific studies that validate the traditional uses of Randia species and evaluate their phytochemical composition have been conducted in Mexico, Brazil, Panama, and the United States of America. Mexico has the highest number of scientific publications (21), followed by Brazil (5), Panama (1), and the United States of America (1).

Ethnobotany of Randia. Reports of traditional uses were found for 12 species of Randia (e.g., antivenom and to treat dysentery, kidney ailments, and cancer) (Table 1), and scientific studies of biological activities (e.g., antioxidant, antimicrobial, antivenom) were reported for nine of them (8.5 %) (Table 1).

Table 1 Traditional uses and demonstrated biological activities of Randia species. 

Plant Part of the plant/ traditional uses Demonstrated biological activities
Randia aculeata L. Fruit/ Against the snake’s bites1 Antinociceptive2, antifungal3, antivenom1,4, nematicide5, toxicity2
Randia armata (Sw.) DC. Leaves/ Leaf decoction to sleep better6 Antioxidant8, antiparasitic7
Randia capitata DC. Not specified/ To treat cough9 ND
Randia cinerea (Fernald) Standl. Fruit and leaves/ To clear the urinary tract (bladder and kidneys)9 ND
Randia echinocarpa Moc. & Sessé ex DC. Fruit/ To treat cancer, malaria, diabetes, peptic ulcers, and diseases of kidney, circulatory and lung 10 Antibacterial11, antidiabetic12,13, antimutagenic14,15, antioxidant13,14,16, cicatrizing17, diuretic18, nematicide19, antiproliferative16, toxicity20
Randia ferox (Cham & Schltdl) DC. Leaves/ To treat diarrhea, intestinal colic and pneumonia21 Antioxidant, cytotoxicity and genotoxicity22
Randia hebecarpa Benth. Stem-roots/ Infusion to treat rheumatism23 Antioxidant and antiinflammatory24
Randia laevigata Standl. Fruit/ To treat gastric discomforts and malaria25 ND
Randia longiloba Hemsl. Bark/ Infusion to treat dengue26 Antifungal3 and nematicide5
Randia monantha Benth. Fruit/ Against bites of snakes and other poisonous animals27 Antioxidant28 and toxicity27
Randia nítida (Kunth) DC. Vegetative parts/ To heal wounds, antiinflammatory, and antispasmodic29,30 Antifungal31
Randia tetracantha (Cav.) DC. Fruit/ To treat dysentery9 ND

1Gallardo-Casas et al. 2012, 2Pérez-Espinosa et al. 2015, 3Gamboa-Angulo et al. 2008, 4Torres-Schwartz et al. 2018, 5Cristóbal-Alejo et al. 2006, 6Zamora-Martínez & Nieto de Pascual-Pola 1992, 7dos Santos et al. 2013, 8Chaves et al. 2015, 9Borhidi & Diego-Pérez 2008, 10Bye et al. 1991, 11Salinas-Sánchez et al. 2009, 12Alarcón-Aguilera et al. 1998, 13Cuevas-Juárez et al. 2014, 14Santos-Cervantes et al. 2007, 15Cano-Campos et al. 2011, 16Montes-Avila et al. 2018, 17Pérez et al. 1993, 18Vargas-Solís & Pérez-Gutiérrez 2002, 19López-Aroche et al. 2008, 20Gil-Avilés et al. 2019, 21Carvalho 2008, 22Pappis et al. 2021, 23Agra et al. 2008, 24Nazari et al. 2006, 25Irigoyen-Rascón & Paredes 2015, 26Trejo-Torres et al. 2014, 27Méndez-Valenzuela & Hernández-Martínez 2009, 28Juárez-Trujillo et al. 2018, 29Erbano & Duarte 2011, 30Pott & Pott 1994, 31Cruz-Silva et al. 2016, ND: Not determined.

Phytochemical studies on Randia. Eight species of Randia have been studied by qualitative phytochemical screening to establish the presence of families of compounds. R. armata (Sw.) DC., R. echinocarpa, R. laevigata, and R. nitida (Kunth) DC are the best studied, and their main families are phenolic acids, flavonoids, terpenes/sterols, and saponins (Table 2). On the other hand, identification of specific compounds has been reported in seven research papers for six species (R. aculeata L., R. echinocarpa, R. ferox (Cham & Schtdel) DC., R. hebecarpa Benth, R. matudae Lorence & Dwyer, R. monantha Benth.) (Table S1, Figure S1). One hundred compounds have been characterized in Randia: 32 phenolic acids, 28 terpenes, three sterols, one alkaloid, and 36 others (sugars, fatty acids, aldehydes, alcohols, and ketones). Most compounds were characterized by liquid chromatography or gas chromatography coupled with mass spectrometry (UPLC-MS/MS or GC-MS). However, compounds of R. echinocarpa have been purified and characterized by instrumental techniques (e.g., infrared, mass spectrometry, nuclear magnetic resonance). Several identified compounds in Randia have shown a range of biological activities (e.g., anticancer, antiinflammatory, antimicrobial) (Table S2) that could support some of their traditional uses.

Table 2 Phytochemical screening test in some species of the genus Randia. 

Species1 Extract/ Fraction Alkaloids Coumarins Flavonoids Tannins Saponins Terpenes/ sterols Free anthracenic derivatives Phenolics Anthraqui-nones
Randia echinocarpa Moc. & Sessé ex DC. 4,a ME - + + + +++ + - ND ND
HF - + - - ++ ++ - ND ND
CF - - + + + ++ - ND ND
AQF - + + + - - + ND ND
AEF - - + + - - ++ ND ND
Randia nitida (Kunth) DC.3,a ME ++ ++ +++ +++ + +++ ND +++ ND
HF - - + - - +++ ND - ND
DMF ++ ++ ++ - - ++ ND +++ ND
AEF ++ ++ +++ ++ + ++ ND +++ ND
Randia laevigata Standl.5,a HE - ND - + + ND ND - -
DME - ND - - + ND ND - -
ME +++ ND +++ - +++ ND ND +++ +++
Randia aculeata L. 6,c ME ND ND + ND + ND ND ND ND
Randia. mira Dwyer 2,b CE - ND ND ND ND ND ND ND ND
Randia altiscandens (Ducke) C.M. Taylor 2,b CE ++ ND ND ND ND ND ND ND ND
Randia aculeata L.2,b CE + ND ND ND ND ND ND ND ND
Randia armata (Sw.) DC. 2,b,* CE +++ ND ND ND ND ND ND ND ND
Randia lasiantha (Standl.) Standl. 2,b CE + ND ND ND ND ND ND ND ND

1Species with highest diversity of compounds is ordered first. 2Soto-Sobenis et al. 2001; 3Cruz-Silva et al. 2007; 4Cano-Campos et al. 2011; 5Jiménez-Ortega et al. 2020; 6Martínez-Ceja et al. 2022. CE, chloroform extract; CF, chloroform fraction; DME, dichloromethane extract; DMF, dichloromethane fraction; EAF, ethyl acetate fraction; HE, hexane extract; HF, hexane fraction; ME, methanol extract. aThe relative quantity of metabolite is established as abundant (+++), moderate (++), poor presence (+), and complete absence (-); bIt is shown the intensity of the orange developed, color ranges from light (+) to very dark (++++); c + indicates presence; - indicates absence; ND, not determined.

Biological activities. Considering the ethnobotanical uses of Randia, fruit was the main employed part reported for 12 species (Table 1, Figure 1). On the other hand, scientific studies of nine species register 14 biological activities, and Randia echinocarpa is the most studied (Appendix 1). Seven documents show the antimicrobial and antiparasitic activities of five species; six studies indicate the antioxidant activity of four species; and three papers study the toxicity of three species. On the other hand, compounds identified in Randia have antioxidant, antiinflammatory, antimicrobial, and antiobesity properties. Such properties have been associated with chronic-degenerative and infectious diseases; thus, these compounds could be responsible for the ethnobotanical uses and demonstrated biological activities of samples obtained from species of Randia (Table S2).

Figure 1 Fruit of Randia species employed in traditional medicine: (A) Randia aculeata, (B) Randia armata, (C) Randia echinocarpa, (D) Randia longiloba, (E) Randia monantha, and (F) Randia obcordata. Images from iNaturalist.org, credits: (a) Minerva Reyes, (b) Hailen Ugalde, (d) Joaquín Cauich Pool, (e) Alfredo Dorantes Euan, and (f) Lex García. 

Discussion

Mexico has the highest number of species richness, endemism, and publications of Randia, parameters that must be associated.

Ethnobotany of Randia. This review shows that most Randia species have not been studied. However, ethnobotanical reports about traditional medicine uses are indicated for 12 species (Table 1). Bye et al. (1991) studied the ethnobotany of Randia echinocarpa, through systematical collection of data and plant specimens from markets in Mexico City. Their results show that R. echinocarpa is known by different common names depending on the country region: granjel is the most common, and others are kakawari, telocoche, xacua, and papache. The most common traditional use of R. echinocarpa is to treat renal diseases, including renal pain, kidney stones, and cystitis. In Mexico, the entire fruit is prepared as infusion or decoction and consumed three times per day or instead of drinking water. Fruit or leaf infusions of R. echinocarpa are also used to treat cough, circulatory ailments, diabetes, diarrhea, malaria, and stomach and intestine cancers.

Gallardo-Casas et al. (2012) reported the traditional medicinal use of Randia aculeata L. in Japama, Veracruz, Mexico, to treat snake bites (Table 1). The plant common names are “crucetillo” or “crucetillo macho”. Fruit is used to prepare drinks, seven fruits (sometimes including the peel) are mixed with 1 L of cherry wine, beer, or cane liquor for one week. This preparation is used orally or topically against the venoms of Bothrops asper, Crotalus spp., Micrurus spp., Apis spp., Latrodectus spp., and Centruroides spp. Randia monantha is distributed in Mexico and Central America, where it is employed to treat snakebites (Méndez-Valenzuela & Hernández-Martínez 2009, POWO 2019). In some communities of Veracruz, Mexico, R. monantha is commonly known as crucetillo and used against the Bothrops asper venom and other poisonous animal bites. The ripe fruit with or without peel is mixed with cane liquor and left to stand. The employed dose depends on the bite or sting of the poisonous animal. This preparation is known since the first settlers’ medicine cabinet of those localities (Méndez-Valenzuela & Hernández-Martínez 2009).

Randia armata is distributed in Mexico and South America, where leaves decoction is employed to better sleep (Zamora-Martínez & Nieto de Pascual-Pola 1992, POWO 2019). Chaves et al. (2015) studied the chemical composition and antioxidant activity of R. armata in four communities in the Buriti dos Montes and Cocal municipalities, Piauí, Brazil; this species is usually consumed as food. The common name of R. armata is taturapé, and the fruit pulp is consumed directly. Another study analyzed the use of R. armata by the ethnic group Chayahuia from Peru; in its medical system, this plant is commonly known as Kahpari werun, and its leaves are used to treat diarrhea. Leaves are prepared by decocting for 0.5 h to drink three times per day (Odonne et al. 2013).

Randia hebecarpa is native to South America, where it is employed as traditional medicine in Brazil, Colombia, Guyana, and Paraguay (Nazari et al. 2006, POWO 2019). Agra et al. (2008) reported that R. hebecarpa is used to treat rheumatism in the Northeast region of Brazil, where it is known as “limaozinho”.

Randia nitidia is distributed in Brazil, Colombia, Ecuador, Guyana, Paraguay, Peru, and Venezuela. Plant preparations have been traditionally used for wound healing and as antiinflammatory and antispasmodic agent. R. nitida has several common names: “indigoberry”, “roseta (rosete”), or “veludo-despinho” (Pott & Pott 1994, Erbano & Duarte 2011, POWO 2019).

Randia ferox is distributed in Argentina, Brazil, and Paraguay, where it has been traditionally employed to treat diarrhea, intestinal colics, and pneumonia; R. ferox is commonly known as “limao-do-mato” or “limoneiro-do-mato” (Carvalho 2008, POWO 2019). The infusion of the leaves is traditionally employed to treat diarrhea, intestinal colics, and pneumonia (Carvalho 2008).

Medicinal uses of other species of Randia are reported. Randia longiloba Hemsl. is endemic to Southwestern Mexico, and its bark infusion has been traditionally employed to treat dengue (Trejo-Torres et al. 2014, POWO 2019). Randia capitata DC. to treat cough and is commonly known as “zapote prieto" (Borhidi & Diego-Pérez 2008); R. tetracantha (Cav.) DC. to treat dysentery and is known as “cruzetillo” (Borhidi & Diego-Pérez 2008). Randia cinerea (Fernald) Standl. is distributed in Mexico, Guatemala, and Honduras, where is known as “crucetillo”, “crucillo”, “rangel”, or “caporal and used to clean the urinary tract (Borhidi & Diego-Pérez 2008, POWO 2019).

Phytochemical studies on Randia. Most Randia species have not been characterized, but the first chemical studies appeared in the 1990s and were conducted on R. echinocarpa (Bye et al. 1991). The qualitative phytochemical studies are limited and incomplete for eight species, being flavonoids and tannins the most found (Table 2). Moreover, compounds have been isolated and identified only in six Randia species (Table S1 and Figure S1) (Nazari et al. 2006, Setzer et al. 2006, Cano-Campos et al. 2011, Juárez-Trujillo et al. 2018, Pappis et al. 2021, Martínez-Ceja et al. 2022), and many of them have demonstrated biological activities (Table S2). The following paragraphs describe the main compounds identified in Randia, and bold numbers in parentheses after the compound name correspond to the respective structure in Figure S1.

Phenolics.- The phenolic compounds in Randia are numerous and include flavonoids, coumarins, and phenolic acids (e.g., phenylpropanoids) (Table S1 and Figure S1). The seeds of R. monantha have the highest phytochemical compound diversity, and the most representatives are the following: flavonoids, e.g., rutin (9); coumarins, e.g., scopoletin (12); phenylpropanoid acids, e.g., chlorogenic acid (16); and phenolic acids, e.g., vanillic acid (22) (Juárez-Trujillo et al. 2018). Phenolic acids are the main compounds in flower essential oil of R. matadue: benzyl benzoate (25) and trans-methyl isoeugenol (30) (Setzer et al. 2006). Kaempferol glycosides (3-6) are abundant in R. hebecarpa (Nazari et al. 2006). Phenylphosphonic acid (32) is identified in leaves of R. aculeata (Martínez-Ceja et al. 2022).

Terpenes.- The species of Randia contain terpenes (Table S1 and Figure S1). In the flowers’ essential oil of R. matudae the main terpenes are oxygenated monoterpenes (46 %) and sesquiterpenes (2.3 %), highlighting the presence of the monoterpenes α-terpineol (41) and linalool (47) (Setzer et al. 2006). Two triterpene saponins are identified in the ethyl acetate and hydromethanolic fractions of R. hebecarpa leaves: cincholic acid 3-O-β-D-quinovopyranosil-28-O-β-D-glucopyranoside (53) and quinovic acid 3-О-β-quinovopyranosyl-28-О-β-D-glucopyranoside (54) (Nazari et al. 2006). In the ethyl acetate fraction of the R. echinocarpa fruit, five triterpenes are identified, being the most abundant quinovic acid (57) and oxoquinovic acid (56) (Bye et al. 1991, Cano-Campos et al. 2011). In the hexane, dichloromethane, and methanol extracts of R. aculeata leaves were identified the diterpene phytol (52) and triterpenes squalene (59) and cycloartenol (60) (Martínez-Ceja et al. 2022).

Sterols.- Randia echinocarpa and R. aculeata are the only species where sterols have been reported (Bye et al. 1991, Cano-Campos et al. 2011, Martínez-Ceja et al. 2022). In the hexane fraction of R. echinocarpa fruits and the hexane, dichloromethane, and methanol extracts of R. aculeata leaves are identified three sterols, and β-sitosterol (61) is the most abundant (Table S1 and Figure S1) (Cano-Campos et al. 2011, Martínez-Ceja et al. 2022).

Others.- Other identified compounds in Randia species are sugars, fatty acids, aldehydes, alcohols, and ketones (Table S1 and Figure S1). The main fatty acids in the essential oils of seeds of R. monantha are linoleic (69), oleic (71), and palmitic (67) (Juárez-Trujillo et al. 2018). The fruit pulp of R. echinocarpa contains linoleic (69) and palmitic (67) acids, and the last one is the most abundant (Cano-Campos et al. 2011). The main alcohols in flower essential oils of R. matudae are cis-3-hexenol (78) and trans-3-hexenol (79) (Setzer et al. 2006). Three aldehydes have been registered for R. echinocarpa, being pentadecanal (97) the most abundant (Cano-Campos et al. 2011). The mannitol (81) has been identified in R. echinocarpa and R. hebecarpa (Bye et al. 1991, Nazari et al. 2006, Cano-Campos et al. 2011). The main polyalcohols in the leaves extracts of R. aculeata are ribitol (85) and glucitol (86) (Martínez-Ceja et al. 2022).

Biological activities. Among the biological activities demonstrated for the 12 species of Randia used in traditional medicine, the antioxidant activity is reported for five species (Table 1 and Appendix 1). Oxidative stress and inflammation have been associated with the etiopathogenesis of different diseases (e.g., cancer, cardiovascular, metabolic, neurodegenerative), and plant antioxidants can be health protective by preventing lipid oxidation, protein denaturation, DNA damage, and improving the DNA repair and detoxification mechanisms (Munialo et al. 2019). Phenolics and flavonoids are common components of Randia (Table S1); these compounds have been proposed as an adjuvant therapy to treat inflammation, activity associated with the antioxidant activity and inhibition of enzymes involved in the production of eicosanoids (Hussain et al. 2016). Therefore, the antioxidant activity of Randia compounds could be relevant in the prevention and treatment of diseases. In general, biological activities demonstrated for Randia support some of their traditional uses (Table 1 and Appendix 1). Randia echinocarpa has been the most studied species. It is endemic to Mexico, where it has been used to treat cancer, malaria, diabetes, and peptic ulcers, as well as renal, circulatory, and pulmonary diseases (Bye et al. 1991). The acetone extracts of stems/leaves of R. echinocarpa have low activities against Staphylococcus aureus, Streptococcus faecalis, Escherichia coli, Proteus mirabilis, Salmonella enterica serovar Typhi, and Candida albicans; the Minimal Inhibitory Concentrations (MIC) are ( 8 mg/mL (Salinas-Sánchez et al. 2009); besides, the fruit acetone extract shows nematicidal activity against Haemonchus contortus L3, inducing up to 37 % death after incubation for 48 h (López-Aroche et al. 2008). Moreover, the aqueous extract of R. echinocarpa has antimutagenic activity in Salmonella enterica serovar Typhimurium YG1024, acting by desmutagenic (damage prevention) and bioantimutagenic (damage repair) mechanisms. In this regard, a bioguided assay of an antimutagenic methanolic extract of R. echinocarpa showed greater activity in its hexane fraction, and the responsible compounds were β-sitosterol, linoleic acid, and palmitic acid (Santos-Cervantes et al. 2007, Cano-Campos et al. 2011). Aqueous and non-polar extracts of R. echinocarpa fruit showed similar antioxidant activities by the β-carotene discoloration method; the aqueous extract has low content of phenolics and authors suggested that synergic effects (e.g., between β-sitosterol and phenolics) are contributing with the antioxidant activity of R. echinocarpa (Santos-Cervantes et al. 2007). The insoluble melanins of R. echinocarpa fruit have high antioxidant activity by the FRAP (1,098.41 ± 11.43 μmol TE/g, TE means Trolox Equivalents) and ABTS (1,333.5 ± 8.45 μmol TE/g) methods. They show cellular antioxidant activity in the Saccharomyces cerevisiae BY4741 strain (Montes-Avila et al. 2018). A dose-response effect was observed with better results at the two lowest melanin concentrations (0.01 and 0.1 mg/mL) than with ascorbic acid. Melanins are ubiquitous biological pigments produced by oxidation and polymerization of phenolics, and in alive organisms are involved in thermoregulation, chemoprotection, camouflage, sexual attraction, and photoprotection (Bilinska 1996, Krol & Liebler 1998). It must be emphasized that melanin-containing food has been associated with antioxidant and immunostimulatory properties (Pugh et al. 2005, Huang et al. 2011). In particular, the insoluble melanins of R. echinocarpa fruit showed immunomodulatory activity by increasing the splenocyte proliferation, and authors suggested that the immunostimulant effect was due to phenolic structures in melanins (Montes-Avila et al. 2018). It was suggested that phenolics induce endogenous enzymes (e.g., superoxide dismutase, catalase, glutathione peroxidase) and chelate metals (e.g., iron and copper) (Montes-Avila et al. 2018).

Soluble melanins (impure and purified) from fruit of Randia echinocarpa have shown a higher α-glucosidase inhibitory activity (αGI) than acarbose, a drug commonly employed to treat type II diabetes (Cuevas-Juárez et al. 2014). Furthermore, the purified melanins showed the highest αGI, suggesting that the components/structure of soluble melanins are essential for the activity. The αGI values were not correlated with the content of phenolics or antioxidant activity, albeit these three parameters increase with purification; consequently, sample composition is differentially affecting such parameters (Cuevas-Juárez et al. 2014). However, fruit decoction of R. echinocarpa did not show anti-hyperglycemic activity in rabbits (Alarcón-Aguilera et al. 1998). Thus, R. echinocarpa extracts have antioxidant, immunomodulatory, and antimutagenic activities that have been considered essential to treat various diseases, including malaria and cancer (Munialo et al. 2019), and support the traditional uses of the species. Supporting the potential of R. echinocarpa as a source of phytotherapeutic compounds, toxicity assays in mice showed that soluble melanins from fruit were innocuous, and treated mice showed normal behavior, weight, and healthy organs (Gil-Avilés et al. 2019).

Randia hebecarpa is traditionally used to treat rheumatism (Nazari et al. 2006). The methanol extract of leaves and its fractions have in vitro antioxidant activities evaluated by the DPPH (2,2-diphenyl-1-picrylhydrazyl) and linoleic acid peroxidation methods. Activities of the methanol extract, ethyl acetate fraction, and hydroxymethanol fraction were similar to the positive control butylated hydroxytoluene (inhibition percentage of 89.4 %) in linoleic acid peroxidation. In the DPPH method, ethyl acetate fraction shows the best activity (IC50 = 60.8 µg/mL). In the most active fractions were identified five flavonoids, two triterpenes, and mannitol. Authors suggested that flavonoids are responsible for antioxidant activity (Nazari et al. 2006). The methanol extract of R. hebecarpa leaves is active against Mycobacterium tuberculosis (250 < MIC < 500 µg/mL) (Araujo et al. 2014) and lacks antiinflammatory activity in the carrageenan or dextran murine models (Nazari et al. 2006).

Randia monantha is traditionally employed to treat snakebites (Méndez-Valenzuela & Hernández-Martínez 2009). The aqueous, methanol, and ethanol extracts of pulp and seeds of their fruits show high in vitro antioxidant activity evaluated by the ABTS (2,2'-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)), DPPH, FRAP (Ferric Reducing Antioxidant Power), and reducing power methods; seed extract shows higher DPPH activity than pulp extract, and it is suggested that flavonoids are the active compounds (Juárez-Trujillo et al. 2018). By contrast, the aqueous extract of pulp was more active than that of seeds by the FRAP method, proposing that pulp antioxidant activity was due to the synergy of phenolics, vitamin C, and melanins (Juárez-Trujillo et al. 2018).

The ethanol extract of R. aculeata fruit is effective against the venoms of the Crotalus simus and Bothrops asper snakes: the extract decreases the tissue damage of skeletal and cardiac muscles and the loss of red blood cells (Gallardo-Casas et al. 2012). It is suggested that extract inhibits the proteolytic enzymes involved in the venom hemotoxic effects. The R. aculeata ethanol extract was also useful as an adjuvant of the polyvalent drug therapy in mice lung tissue against the Bothrops asper venom (Torres-Schwartz et al. 2018). Compared with venom-treated mice, mice treated with venom followed by the polyvalent serum had decreased atrophy and bleeding in the lungs. However, those treated with venom, polyvalent serum, and extract did not show these symptoms. Therefore, it was suggested that extract neutralizes the venom toxins. The ethanolic extract of R. aculeata was innocuous in mice (LD50 > 1,000 mg/kg b.w.) and was able to reduce the number of acetic acid-induced contortions, thus suggesting that it has an analgesic effect at the visceral level (Pérez-Espinosa et al. 2015). Martínez-Ceja et al. (2022) evaluated the in vitro antiinflammatory, antibacterial, and antioxidant activity of methanol, hexanic, and dichloromethane extracts of Randia aculeate leaves. At the tested concentrations, none of the extracts showed activity against Staphylococcus aureus, Staphylococcus aureus-MRSA, Streptococcus pyogenes, Escherichia coli, and Salmonella Typhimurium. The methanol extract of Randia aculeata showed high in vitro antioxidant activity with the following IC50 values: 92.92 ± 0.91 µg/mL in DPPH and 14.27 ± 0.20 µg/mL in ABTS. The extracts did not affect the RAW 267.4 cells viability and showed a concentration-dependent inhibition of the nitric oxide (NO) production, being most active the hexane (26.25 ± 2.62 % at 20 µg/mL) and dichloromethane (35.38 ± 4.35 % at 40 µg/mL) extracts. It is suggested that Randia aculeata may be a promising medicinal resource.

Randia armata is traditionally employed to better sleep (Zamora-Martínez & Nieto de Pascual-Pola 1992). An ethanol-water (7:3 v/v) extract of R. armata aerial parts shows moderate antiparasitic activity against Larvae of Rhipicephalus (Boophilus) microplus (75 % efficacy at 40 % extract concentration) (dos Santos et al. 2013). In addition, the in vitro antioxidant activity of the methanolic extract of R. armata has been high due to its elevated concentration of phenolics and carotenes (Chaves et al. 2015).

Randia nitida is traditionally used for wound healing (Pott & Pott 1994, Erbano & Duarte 2011). Methanolic extract of leaves and its fractions show antifungal activity against Colletotrichum truncatum, Rhizoctonia solani, and Sclerotinia sclerotiorum. This activity may be related to their main flavonoid, steroid, and triterpene components (Cruz-Silva et al. 2016).

Randia longiloba has been traditionally employed to treat dengue (Trejo-Torres et al. 2014). The ethanol extract of leaves, stems, and roots of R. longiloba show nematicidal activity (Cristóbal-Alejo et al. 2006).

Randia obcordata S. Watson is distributed from Texas to Venezuela, and it has no information on medicinal uses (POWO 2019) nor phytochemical characterization. The ethanol extract of R. obcordata leaves inhibits the growth of the fungi Alternaria tagetica, Colletotrichum gloeosporioides, and Rhizopus sp. In contrast, the root extract only inhibits the growth of Rhizopus sp. (Gamboa-Angulo et al. 2008). In addition, the ethanol extracts of leaves, stem, and roots of R. obcordata were nematicidal against Meloidogyne incognita J2, and the highest mortality was obtained with the extract of leaves (60 % at 500 ppm) (Cristóbal-Alejo et al. 2006).

Randia ferox is traditionally employed to treat diarrhea, intestinal colics, and pneumonia (Carvalho 2008). The aqueous extract de R. ferox leaves show high in vitro antioxidant DPPH activity (IC50 = 79.26 µg/mL). The cytotoxicity and genotoxicity of the R. ferox extract were evaluated in different cell lines. Peripheral blood mononuclear cells treated for 24 h showed normal cell viability. All evaluated concentrations reduced the Reactive Oxygen Species (ROS) levels without affecting the Nitric Oxide (NO) levels. In addition, most tested concentrations did not affect the release of double-strand DNA (dsDNA). Thus, it is suggested that aqueous extract R. ferox is safe and has the potential to treat diverse illnesses/ symptoms (Pappis et al. 2021).

Increasing knowledge about phytochemical composition and biological activities is necessary to produce high-value products through modern biotechnological tools. Based on the demonstrated characteristics of R. echinocarpa, plant cell tissue culture was employed to produce calli and plantlets toward the in vitro production of antioxidants and other bioactive metabolites (Valenzuela-Atondo et. al. 2020).

Supplementary material

Supplemental data for this article can be accessed here: https://doi.org/10.17129/botsci.3004

Supplementary material

Acknowledgments

The authors acknowledge the financial support by the National Council for Science and Technology, Mexico (CONACYT A1-S-32946) and “Programa de Fomento y Apoyo a Proyectos de Investigación”, Autonomous University of Sinaloa (PROFAPI PRO_A2_011), CONACYT-scholarship to Manrique Ojeda-Ayala, and academic advice by Dr. Rito Vega-Aviña, School of Agronomy, Autonomous University of Sinaloa.

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Appendix 1.

Biological activities of extracts and compounds of Randia species. 

Biological activity Plant Part of the plant Type of extract/Preparation Model/Method Result Reference
Antibacterial Randia echinocarpa Moc. & Sessé ex DC. Leaves and stems AE Staphylococcus aureus, Streptococcus faecalis, Escherichia coli, Proteus mirabilis, Salmonella Typhi and Candida albicans MIC = 8 mg/mL for S. aureus and S. faecalis, MIC > 8 mg/mL for the rest Salinas-Sánchez et al. 2009
Randia aculeata L. Leaves ME, HE and DME Staphylococcus aureus, Staphylococcus aureus-MRSA, Streptococcus pyogenes, Escherichia coli and Salmonella Typhimurium None of extracts had an inhibitory affect Martínez-Ceja et al. 2022
Randia hebecarpa Benth. Leaves ME Mycobacterium tuberculosis MIC > 250 μg/mL Araujo et al. 2014
Antiparasitic Randia armata (Sw.) DC. Plant HEE Larvae of Rhipicephalus (Boophilus) microplus 25, 28, and 75 % efficacy at [5], [20] and [40] % of HEE dos Santos et al. 2013
Antifungal Randia longiloba Hemsl. Leaves EE Alternaria tagetica, Colletotrichum gloeosporioides, Fusarium oxysporum and Rhizopus sp. Only active against Rhizopus sp. Gamboa-Angulo et al. 2008
Randia obcordata S. Watson Stems and root EE Alternaria tagetica, Colletotrichum gloeosporioides, Fusarium oxysporum, and Rhizopus sp. Effect against A. tagetica, F. oxysporum and Rhizopus sp.
Randia aculeata var. aculeata L. Leaves and root
Randia nitida (Kunth) DC. Leaves ME, HF, DMF, and EAF Colletotrichum truncatum, Rhizoctonia solani Kühn and Sclerotinia sclerotiorum Activity order was as follows: EAF>DMF>HF, evaluated at [160 µg/mL] Cruz-Silva et al. 2016
Nematicide Randia echinocarpa Moc. & Sessé ex DC. Flowers AE Haemonchus contortus L3 Effect at [20 mg/mL], % larval mortality 3.33 ± 1.76, 37 ± 11.83, and 25.33 ± 3.38 after 24, 48, and 72 h respectively López-Aroche et al. 2008
Randia longiloba Hemsl. Leaves, root, and stems EE Meloidogyne incognita J2 The EE of leaves induced higher mortality at 72 h: 95% at 500 ppm and 25% at 250 ppm Cristóbal-Alejo et al. 2006
Randia obcordata S. Watson The EE of stems induced higher mortality at 72 h, 63% at 500 ppm
Randia aculeata L. var. aculeata The EE of leaves show higher % mortality of 95 and 8 at [500] and [250] ppm at 72 h
Antioxidant Randia echinocarpa Moc. & Sessé ex DC. Fruit ME, HE, CE, and AQE β-carotene bleaching AQE showed the highest AA in vitro Santos-Cervantes et al. 2007
Partially purified soluble melanins ABTS and FRAP High AA in vitro Cuevas-Juárez et al. 2014
Purified insoluble melanins FRAP, ABTS and Saccharomyces cerevisiae High AA in vitro and showed no dose-response effect on the oxidizing agent H2O2 Montes-Avila et al. 2018
Randia ferox (Cham & Schltdl) DC. Leaves AQE DPPH High AA in vitro Pappis et al. 2021
Randia aculeata L. Leaves ME, HE and DME DPPH and ABTS High AA in vitro Martínez-Ceja et al. 2022
Randia hebecarpa Benth. Leaves ME, AQF, HF and EAF DPPH and linoleic acid peroxidation ME, AQF, and EAF showed the same effect as BHT, and EAF had the best IC50 = 60.8 µg/mL Nazari et al. 2006
Randia monantha Benth. Pulp and seed ME and EE FRAP, DPPH, ABTS and reducing power. High AA in vitro Juárez-Trujillo et al. 2018
Randia. armata (Sw.) DC. Pulp HME DPPH and ABTS High AA in vitro Chaves et al.2015
Anti-inflammatory Randia hebecarpa Benth. Leaves ME Albino rats No significant effect on inflammation reduction Nazari et al. 2006
Randia aculeata L. Leaves ME, HE and DME RAW 264.7 cell line All extracts showed a dose-dependent effect in the inhibition of NO production Martínez-Ceja et al. 2022
Cicatrizing Randia echinocarpa Moc. & Sessé ex DC. Fruit AQE, CE, and BE Wistar rats AQE increased healing and clotting time Pérez et al. 1993
Antidiabetic Randia echinocarpa Moc. & Sessé ex DC. Fruit Aqueous decoction Rabbits Not significant decrease in hypoglycemic peak Alarcón-Aguilera et al. 1998
Partially purified soluble melanins Inhibition of α-glucosidase High inhibition of α-glucosidase IC50= 1.00 ± 0,010 and 1.17 ± 0.069 mg / mL extracted at room and boiling temperature, acarbose IC50= 8.38 mg / mL. Cuevas-Juárez et al. 2014
Antimutagenic Randia echinocarpa Moc. & Sessé ex DC. Fruit AQE Salmonella enterica serovar Typhimurium YG1024 Inhibited the 1-NP mutagenicity by 32 and 56% Santos-Cervantes et al. 2007
ME, AQF, HF, EAF, and CF Salmonella enterica serovar Typhimurium YG1024 The HF was the most active and contains palmitic acid, linoleic acid, and β-sitosterol compounds Cano-Campos et al. 2011
Proliferative Randia echinocarpa Moc. & Sessé ex DC. Fruit Purified insoluble melanins Splenocytes of BALB/c mice It showed a significant difference of [25 µg/mL] with respect to LPS and PHA positive controls Montes-Avila et al. 2018
Diuretic Randia echinocarpa Moc. & Sessé ex DC. Fruit AQE Wistar rats Increased urine volume Vargas-Solís & Pérez-Gutiérrez 2002
Antinociceptive Randia aculeata L. Fruit EE Wistar rats Analgesic effect at visceral level Pérez-Espinosa et al. 2015
Antivenom Randia aculeata L. Fruit EE CD1 mice Decreased atrophy and bleeding in the lungs Torres-Schwartz et al. 2018
Decreased tissue damage and red blood cells Gallardo-Casas et al. 2012
Toxicity Randia monantha Benth. Fruit, leaves, and stems EE Artemia salina L. No toxicity up to 1 mg/mL Méndez-Valenzuela & Hernández-Martínez 2009
Randia aculeata L. Fruit EE Mice No toxicity up to 1000 mg/kg b.w. Pérez-Espinosa et al. 2015
Randia echinocarpa Moc. & Sessé ex DC. Fruit Partially purified soluble melanins BALB/c mice No toxicity up to 5 g/kg b.w. Gil-Avilés et al. 2019
Cytotoxicity and Genotoxicity Randia ferox (Cham & Schltdl) DC. Leaves AQE Cell lines Vero, RAW 267.4 HFF-1, and U-87 MG The extract did not affect cellular proliferation, decreased ROS, and increased NO. Pappis et al. 2021
Extract concentration did not affect dsDNA release compared to untreated cells

AA, antioxidant activity; AE, acetonic extract; AQE, aqueous extract; AQF, aqueous fraction; BE, benzene extract; BHT, butylated hydroxy toluene; CE, chloroformic extract; CF, chloroformic fraction; DME, dichloromethane extract; DMF, dichloromethane fraction; dsDNA, doble stranded DNA; EAF, ethyl acetate fraction; EE, ethanolic extract; HE, hexanic extract; HEE, hydroethanol extract; HF, hexanic fraction; HME, hydromethanol extract; LPS, lipopolysaccharide; ME, methanol extract; NO, nitric oxide; PHA, phytohemagglutinin; ROS, reactive oxygen species.

Received: June 22, 2021; Accepted: December 01, 2021; Published: May 23, 2022

*Corresponding author: fdelgado@uas.edu.mx

Associate editor: Arturo de Nova

Authors’ contribution: MOA, database searching, information analysis, and manuscript preparation; SMGC, manuscript preparation and critical review; FDV, manuscript preparation and critical review.

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