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22 October 2022

An Overview of Genus Malachra L.—Ethnobotany, Phytochemistry, and Pharmacological Activity

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Grupo de Investigación en Química Orgánica Medicinal, Facultad de Ciencias Farmacéuticas, Campus de Zaragocilla, University of Cartagena, Cartagena 130001, Colombia
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Departamento de Ciencias Farmacéuticas, Área de Química Farmacéutica, Centro de Enfermedades Tropicales de la Universidad de Salamanca (CIETUS), Instituto de Investigación Biomédica de Salamanca (IBSAL), Facultad de Farmacia, Campus Miguel de Unamuno, Universidad de Salamanca, 37007 Salamanca, Spain
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Author to whom correspondence should be addressed.
Plants2022, 11(21), 2808;https://doi.org/10.3390/plants11212808
This article belongs to the Special Issue Advances in Research on Plant Natural Products
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Abstract

The genus Malachra L. belongs to the family Malvaceae. It includes herbs or subshrubs of nine accepted species with approximately thirty synonyms, and it has been widely used in community folk medicine to treat health problems including inflammation, nasal obstruction, leishmaniasis, malaria, childbirth, kidney disorders, fever, respiratory tract diseases, among others. From the genus Malachra L., flavonoids, steroids, triterpenes, anthocyanins, leucoanthocyanins, saponins, carbohydrates, phenols, glycosides, and alkaloids have been isolated and identified. Some pharmacological reports have indicated that the genus has antidiarrheal, antiepileptic, antiulcerogenic, antioxidant, anticonvulsant, antiviral, anticancer, antibacterial, anthelmintic, and hepatoprotective properties. However, there have been limited studies of bioactive molecules with pharmacological and biological activities associated with Malachra alceifolia Jacq., Malachra capitata (L.) L., Malachra fasciata Jacq., Malachra radiata (L.) L., Malachra ruderalis Gürke., Malachra rudis Benth., Malachra helodes Mart., Malachra urens Poit. ex Ledeb. & Alderstam., and Malachra officinalis Klotzsch. In this review, we consider the conservation of these species to save the ancestral knowledge of their traditional use in populations, and their pharmacological potential for future studies in search of alternatives for solutions to diseases in humans and animals and tools for the design and search of potential bioactive compounds against infectious and non-infectious agents.

1. Introduction

Various populations of some regions of the world use medicinal plants to cure and prevent their health problems [1]. However, the World Health Organization (WHO) has defined ancestral and traditional knowledge resources obtained from plants, extracts, fractions, or compounds as a primary source for the identification of molecules, substances, or active principles to be used in the development of drugs and phytomedicines for disease prevention [2,3,4]. Secondary metabolites derived from plant species such as Taxus brevifolia (Paclitaxel) [5], Catharanthus roseus (Vincristine) [6], Digitalis lanata (Digoxin) [7], Ephedra distachya (Ephedrine) [8], Artemisia annua (Artemisinin) [9], Salix alba (acetylsalicylic acid) [10], and Papaver somniferum (morphine) [11] have been used as drugs with anticancer, cytotoxic, antimicrobial, analgesic, inflammatory, antiestrogenic, antiallergic, antioxidant, and other activities [12,13]. Note that ancestral and traditional community activities have used medicinal plants for phytotherapy in primary health care and for validation of their ethnopharmacological use [14,15].
There are about 382,000 accepted plant species names in the world [16,17]. The criteria for considering the acceptance, name, and synonyms of a plant species are defined by taxonomic concepts from botanical studies, herbarium specimens, biogeographical, conservation and phylogenomic research, as well as expert observations [18]. About 20% of these names are unresolved, indicating that some included data sources that did not provide any evidence or view on whether or not the name should be treated as accepted, or there were contradictory opinions that could not be easily resolved, leaving ambiguous and unchecked concepts [17].
Malachra L. is an accepted genus that belongs to the Malvaceae family and contains seventeen known species, with only nine accepted species including Malachra alceifolia Jacq., Malachra capitata (L.) L., Malachra fasciata Jacq., Malachra radiata (L.) L., Malachra ruderalis Gürke., Malachra rudis Benth., Malachra helodes Mart., Malachra urens Poit. ex Ledeb. & Alderstam [16], and Malachra officinalis Klotzsch [17]. However, only eight species of the genus Malachra L. are ambiguous and unchecked [7] wih some reports of botanical descriptions, ethnobotanicals, phytoconstituents, pharmacological, and biological activities. Therefore, some species names of the genus Malachra L. are currently unchecked, ambiguous, and awaiting taxonomic scrutiny: Malachra lobata L., Malachra texana A. Gray., Malachra triloba [Desf.], Malachra rosea Hoffmanns., Malachra digitata C. Presl., Malachra urticifolia C. Presl., Malachra viminea Fisch. ex Steud., and Malachra plumosa Desr. [8]; to date, there are no reported descriptions such as those mentioned above [18,19].
The life form of the Malachra L. genus is a herb or subshrub present in terrestrial substrate [19]. Regarding geographical distribution, the genus Malachra L. genus is native to approximately fifty countries in tropical and subtropical America and West Africa, and has been introduced in some regions of the United States, India, and Asia [20]. Colombia and Brazil are biodiverse countries that harbor most of the Earth’s species of the genus Malachra L. and high numbers of endemic species including Malachra alceifolia Jacq., Malachra capitata (L.) L., Malachra fasciata Jacq., Malachra radiata (L.) L., Malachra ruderalis Gürke., and Malachra rudis Benth. are distributed in almost all the territories. In Colombia, there are few studies on the conservation status according to the categories and criteria of the International Union for Conservation of Nature and Natural Resources (IUCN) and biological and pharmacological potentials [21].
The genus Malachra L. contains phytoconstituents isolated from whole plant, leaf, stem, flowers, and root, fresh or dried, flavonoids [22]; compounds of phenolic acids [23,24]; phytosterol [24,25]; fatty acid derivative [26]; alkaloids, tannin [27,28]; and dipeptide [29,30]. The phytoconstituents are molecules necessary for plant survival, but also contribute to the prevention of many infectious and non-infectious diseases. Several communities in these countries use these traditional plants for treating ailments such as inflammation, clogged nose [1], leishmaniasis [31], malaria [32,33], kidney disorder, fever [34], diseases of the respiratory tract [35], and during childbirth, and therefore, have become one of the best medicinal alternatives for these communities.
The species in the genus Malachra L. are frequently reported as weeds, in pastures and rangelands, and usually serving as food for livestock [36]. In addition to this, they fulfill functions of vital importance to the ecosystem, and they are a source of food for various species of butterflies, as well as a great repository for the larvae of the same [37]. At an ecosystemic level, the species in this genus are considered to be primarily for the regeneration processes of intervened ecosystems since they favor the succession processes of other species in these ecosystems [38].
In this review, we organize the ethnobotanical, phytochemical, biological, pharmacological, and toxicological information of plants belonging to the genus Malachra L., to analyze the state-of-the-art of the genus and to highlight the pharmacognostic potential of molecules extracted from these plants, organic extracts, and fractions as potential sources of new drugs and for the development of innovative medicines.

2. Material and Methods

This review was conducted using the Preferred Reporting Items for Systematic Review (PRISMA) guidelines for systematic reviews. First, in accordance with the PICO method of the PRISMA guidelines for data selection, a scientific question was posed with the following heading: P: genus Malachra L. in the family Malvaceae, I: Included species, C: accepted, ambiguous, and unchecked species, O: taxonomy, botanical descriptions, geographical distribution, phytochemistry, ethnobotany, pharmacological, and biological activities of species. Followed by the search strategy: ((Malachra [Title/Abstract])) OR, Search: (Taxonomy [MeSH Terms]) AND (genus Malachra [Title/Abstract])) AND (Taxonomy [Title/Abstract]) OR (Malachra species [Title/Abstract])) AND (Malachra species, ethnobotanical [Title/Abstract])), OR (Malachra species [Title/Abstract]) AND (Malachra species, phytoconstituents [Title/Abstract]) AND (Malachra species, ethnobotanical [Title/Abstract]) AND (Malachra species, pharmacological activity [Title/Abstract]) AND (Malachra species, biological activity [Title/Abstract]); the type of search: new; databases: Medline, Latin America & Iberia; Platforms: PubMed accessed on 10 January 2022 (https://pubmed.ncbi.nlm.nih.gov/, accessed on 1 March 2022), ScienceDirect accessed on 10 January 2022 (www.sciencedirect.com, accessed on 1 March 2022), Scopus accessed on 10 January 2022 (www.scopus.com, accessed on 1 March 2022), and Scielo accessed on 10 January 2022 (www.scielo.org, accessed on 1 March 2022); search date range: unlimited; Language Restrictions: none. Different inclusion and exclusion criteria were considered. The inclusion criteria used were as follows:
The exclusion criteria were those studies that did not meet criteria one, two, and three.
There were fifteen bibliographic registers identified in the database; records deleted eight (congress abstract six, taxonomic website version not updated one (http://www.theplantlist.org/, accessed on 1 March 2022), article without pharmacological description one); articles evaluated for eligibility eight; articles accepted for the study seventy-nine; flora microsites accepted nine; graduate work four.

3. Taxonomy the Genus Malachra

According to World Flora Online, the genus Malachra L. belongs to the family Malvaceae, the group of angiosperms with the largest accepted name reports, including 14,539 scientific species names, 4465 accepted species names, and 245 genera [39]. The botanical characteristics of this family describe its growth as shrub, tree, herb, liana/vine, subshrub, aquatic, terrestrial, hemiepiphytic, and rupicolous [17,40]. The genus Malachra L. has nine species with accepted names and prolific taxonomic synonyms with adjusted morphological descriptions [17]. However, in the Flora World website Malachra officinalis Klotzsch., is accepted, whereas in other flora websites such as https://powo.science.kew.org/, https://wcvp.science.kew.org/, and https://www.tramil.net/es, (accessed on 1 March 2022), this species is not accepted (Table 1 and Table 2). There is no information on this species provided in this review due to its limited studies.
Table 1. Taxonomic name status of species in the genus Malachra L.
Table 2. Taxonomic synonyms for species of the genus Malachra L.

4. Botanical Description of the Species of the Genus Malachra L.

The genus Malachra L. is represented by herbs or suffrutes, sometimes puberulent, generally hispid, or with stinging trichomes. Leaves are simple or palmately lobed; acute, acuminate, or obtuse at the apex; truncated or subcordate at the base; serrated or crenated; and generally pubescent. They also present: bracteate inflorescences; axillary or terminal heads; broadly cordate-ovate bracts at the base, with prominent nerves often alternating with whitish areas, although it can be in other parts green and sessile. Absent calliculus (except in M. radiata); small calyx, five-lobed; white, yellow, or lilac corolla; and five-lobed leaves can also be observed. Additionally, schizocarpal fruits have the shape of a wheel similar to a cheese that can be split into five ripe wing types; flowers are in heads, surrounded by bracts larger than them [17,41,42,43].
Malachra alceifolia Jacq. is a herb or shrub, 1. 6 m tall. The aerial parts and petioles are hispid, simple or split, flavescent, tuberculate base, scattered hairs, short, star-shaped, and long forming knots, with stem pubescence and a green to reddish color. The leaves are simple, opposite, and lobed, with up to five lobes, with pubescence, and their margins are serrated or toothed. There are inflorescences in axillary heads with the presence of acuminate bracts and flowers with five petals, 2 to 3 cm in diameter, with a yellow coloration. The fruits have bracts and persistent calyx, with numerous seeds, up to 2 mm in diameter, dark colored, and flattened (Figure 1) [44].
Figure 1. Malachra alceifolia Jacq.
Malachra capitataLinn. is a herb or subshrub, up to 2 m tall, with stem pubescence and green to orange coloration. The leaves are simple, opposite, palmate or lobed, with up to five lobes; the texture of the leaves is velvety and their margins are crenulate or serrated. Inflorescences are peduncular and axillary, with the presence of lanceolate bracts; flowers have five petals, 1 cm in diameter, with a white coloration. Schizocarpic fruits have single seeds up to 3 mm in diameter, and are dark colored (Figure 2) [45].
Figure 2. Malachra capitata Linn.
Malachra fasciata Jacq. is a herb or subshrub, up to 2 m tall, with stem pubescence, simple or stellate trichomes up to 7 mm, and green to orange coloration. The leaves are simple, opposite, ovate, truncated at the base, acute at the apex, lobed or deeply parted, otherwise crenate-serrate, pubescent above with appressed trichomes. The heads are short-stalked bracts, 2–6 per head, lance/ovate, subcordate at the base, acute at the apex, often ciliate, prominently hispid. Calyx 4 to 5 mm, hispid; petals white 6–8 mm, mericarps light brown to grayish green, reticulate veined (Figure 3) [46].
Figure 3. Malachra fasciata Jacq.
Malachra radiata (L.) L. is a herb or suffrutex, 1.5 m tall, with stem pubescence and green and purple coloration. The leaves are simple, opposite, palmate or lobed, with up to seven lobes; the texture of the leaves is velvety, and their margins are crenulate or serrated, and most apical leaves may have a triangular shape. Inflorescences are pedicular and terminal, with the presence of ovate or acute bracts; flowers have five petals, 2.5 cm in diameter, with a lilac coloration and purple at the base. Schizocarpic fruits have numerous seeds, up to 2 mm in diameter, and are dark colored (Figure 4) [47].
Figure 4. Malachra radiata (L.) L.
Malachra ruderalis Gürke. is an annual herb, up to 3 m high, with stem pubescence and green coloration. The leaves are simple, opposite, palmate or lobed, with up to five lobes; the texture of the leaves is velvety, and their margins are crenulate; the most apical leaves have a triangular shape. It shows pedicular inflorescence with terminal or acute axillary bracts, five petals, 3 cm long, with yellow schizocarpic fruit with numerous dark-colored seeds up to 2 mm in diameter (Figure 5) [48,49].
Figure 5. Malachra ruderalis Gürke.
Malachra rudis Benth. is a perennial herb, up to 0.7 m high, with a stem that has very short pubescence, and its coloration is light green. The leaves are simple, opposite, lobed, with up to three lobes; velvety texture; crenulated margins with pedicular, axillary, or terminal inflorescence; ovate bracts with five petals; 1.5 cm in long. Schizocarpic fruits are yellow to white with numerous seeds up to 1 mm in diameter, one per carpel (Figure 6) [48,49].
Figure 6. Malachra rudis Benth.
Malachra urens Poit. ex Ledeb. & Alderstam is an annual herb, up to 1 m high, with pubescent stems of different sizes and green to orange coloration. The leaves are simple, opposite and lobed, with up to three lobes relatively marked, with pubescence; the margins of the leaves are toothed, about 3–12 cm long. Inflorescences are peduncular racemes with acuminate, boat-shaped, pubescent bracts. Flowers have five petals, 2 to 3 cm in long, with a yellow color. Schizocarpic fruits have mericarps and pubescent bracts, with numerous seeds, up to 2 mm in long, dark colored, and flat (Figure 7) [48,49].
Figure 7. Malachra urens Poit.
Malachra helodes Mart. is an annual herb, up to 1 m high. The stem is slightly pubescent with dark to light green coloration. The leaves are simple, opposite, and lobed, with up to five lobes that are well marked, with slightly marked pubescence on the underside; the margins of the leaves are serrated, about 3–10 cm long. Inflorescences are terminal and axillary racemes with the presence of acuminate bracts in the form of pubescent. The flowers have five petals, 2 to 3 cm in length, with a pink color. Schizocarpic fruits with mericarps and bracts with stem indumentum hispid; terminal inflorescence; pinkish flower; epicalyx absent; fruit, up to 4 mm in length; glabrous indumentum (Figure 8) [48,49].
Figure 8. Malachra helodes Mart. ex Ledeb. & Alderstam.

5. Geographical Distribution of the Genus Malachra L.

The genus Malachra L. is geographically distributed in tropical and subtropical America, west tropical Africa, and Southwest Asia [49].
The species of the genus Malachra L. are native to: South America countries (northeast Argentina, Bolivia, north Brazil, northeast Brazil, southeast Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Peru, Suriname, and Venezuela); Central America countries (Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, and Panama); southwest Caribbean and Bahamas (Aruba, Cuba, Dominican Republic, Haiti, Jamaica, and Trinidad-Tobago); North America countries (Mexico); American Caribbean (Puerto Rico); Africa countries (Benin, Burkina, Congo, Chad, Ivory Coast, Mali, Ghana, Sudan, Niger, Nigeria, Senegal, and Togo); Caribbean Sea Islands (Netherlands Antilles, Leeward Is., Windward Is., and Venezuelan Antilles) [49]. Moreover, the genus has been introduced in: Asian countries (India, Thailand, Bangladesh, Taiwan, Philippine, and Indonesian); United States (Hawaii, Louisiana Florida, and Texas); Caribbean Sea Islands (Guadalupe, Martinique, and Granada) [49] (Figure 9).
Figure 9. Geographical distribution of the genus Malachra L. Colombia and Brazil (green) countries with greater diversityThe countries of Colombia and Brazil have the largest number of species of the genus Malachra L., with six of the nine accepted names (Malachra alceifolia Jacq.; Malachra capitata (L.) L.; Malachra fasciata Jacq.; Malachra radiata (L.) L.; Malachra ruderalis Gürke Benth., with the different species Malachra rudis Benth. present only in Colombia [50] and the species Malachra helodes Mart. present only in Brazil [43]), followed by Peru, Ecuador, and Puerto Rico with five of the nine accepted names, see Table 3 [49,50].
The distribution of the species in Brazil and Colombia covers most of the regions [43,50]. The species with the highest abundance are found in Colombian Caribbean, denoting their preference for warmer climates. In terms of their ecology, they prefer open habitats such as the savannah and scrublands; however, they can occur less frequently in dry and humid forests. There have been a few reports on the conservation status of the species in the genus Malchara L. In this study, in Table 4, only the conservation status of Malachra alceifolia Jacq., in Colombia, is included.
Table 4. Species of the genus Malachra L. occurring in Colombia.

6. Species of the Genus Malachra L. with Ethnobotanical Use

Medicinal plants of traditional use have been included in the Traditional and Complementary Medicine (TCM) report by the World Health Organization (WHO). Many of them are used in developing countries such as Chile and Colombia, with usages of 71% and 40% of the population, respectively [51,52]. Table 5 lists and describes the species of the genus Malachra L. with reported medicinal use, including vernacular name, part of the plant used, condition treated, preparation and administration, and the country where its use has been reported. The species in the genus Malachra L. with the highest reported ethnobotanical use are M. alceifolia Jacq., (for treatment of inflammation, clogged nose, during malaria, childbirth, drunk headache, kidney disorder, fever, and headache), M. capitata (L.) L., (for pain, diarrhea, convulsion, hepatic cirrhosis, inflammation, pyrexia, ulcer, dementia, treatment of wounds, gastric disorders, jaundice, childbirth, malaria headache, and fever), M. fasciata Jacq., (for emollients, hemorrhoids, fever, impotence, gonorrhea, rheumatism, demulcent, and diuretic), M. ruderalis Gürke., (for pulmonary diseases, fever, cough, sore throat, flu, colds, whooping cough, pulmonary diseases, COVID-19, stomach problems, diarrhea, fever, skin spots, skin infections, gastritis, stress inflammation, and vaginal infection).
Table 5. Summary of the species of the genus Malachra L. with reported medicinal use.

7. Phytochemistry Species of the Genus Malachra L.

Phytoconstituents are chemical compounds that plants synthesize as a defense mechanism against biotic and abiotic environmental conditions; they play key roles in biological processes [58,59]. Many phytoconstituents isolated from the genus Malachra L., such as flavonoids, coumarins, carbohydrates, glycosides, triterpenes, alkaloids, tannins, and saponins, exhibit pharmacologic activity. Table 6 lists the phytoconstituents reported only in Malachra species: M. alceifolia Jacq., M. capitata (L.) L., and M. fasciata Jacq, see Figure 10 molecular structure of some compounds isolated from species of the genus Malachra L.
Table 6. Major phytoconstituents identified in species of the genus Malachra L.
Figure 10. Molecular structure of some compounds isolated from species of the genus Malachra L.
Generally, organic compounds obtained from extracts, fractions, and isolated compounds of plant species possess unique structural characteristics among which the geometrical and energetic interactions of the atoms stand out; chirality and stereoisomers of molecular structures, intermolecular interactions, hydrogen bond acceptors and donors, molecular mass, diversity of ring systems, among others, become tools of interest for medicinal chemistry in drug development, to improve the potency, for pharmacokinetic properties, and to reduce the toxicity of new drugs [60]. However, the secondary metabolites isolated from plant species constitute a group of chemical molecules with a great diversity of biological activities applied to the pharmaceutical, cosmetic, and food sectors [61].
Gallic acid (GA) is a phenolic compound with anti-inflammatory, antimicrobial, hepatoprotective, neuroprotective, and carcinogenic properties that prevent gastrointestinal, cardiovascular, metabolic, and neuropsychological diseases [62]. The livers of Wistar rats exposed to carbon tetrachloride in doses of 50 mg/kg and 100 mg/kg GA, were evaluated by decreasing serum liver enzymes, regulating the expression of proinflammatory genes, and regulating the expression of antioxidant genes [63]; mercuric chloride induced at 200 mg/kg, increased glutathione peroxidase, superoxide dismutase, and catalase activity, and decreased the level of glutathione in liver tissue [64]. Caffeic acid has antimicrobial potential against Staphylococcus aureus strains with MICs from 256 µg/mL to 1024 µg/mL [65]. The compound quercetin isolated from extracts and organic fractions of Allium cepa L., Morus alba, Camellia sinensis, Moringa oleifera, and Centella asiatica, at doses between 50 and 100 mg/kg, and evaluated in in vivo models, showed antiulcer activity [66]. Beta-sitosterol isolated chloroform extract of Corchorus capsularis L. leaves has been shown to exhibit a significant effect against trypanothione reductase Leishmania donovani promastigotes at IC50  =  17.7  ±  0.43 µg/mL [67], and the dipeptide aurantiamide acetate patent has an effect of resisting influenza virus and an inhibition effect on a cytopathic effect mediated by the influenza A virus CN106431960B, filing date: 11 November 2018, legal status: active [68].

8. Species of the Genus Malachra L. with Pharmacological Activity

Applications of plant remedies in traditional medicine are still central in the health systems in some countries of world [69]. The biogenesis and biosynthesis of phytoconstituents in plant species provide an opportunity for medicinal chemistry to advance pharmacological studies for treating pathologies that have been little studied [70]. Table 7 summarizes the most important pharmacological activities reported for the genus Malachra L., such as antidiarrheal, anti-epileptic, antiulcerogenic, antioxidant, anticonvulsant, hepatoprotective, antiviral, anticancer, antibacterial, and anthelmintic properties. The bibliographic search describes only the pharmacological activities of M. alceifolia Jacq., M. capitata (L.) L., and M. fasciata Jacq.
Table 7. Summary of the species of the genus Malachra L. with reported pharmacological activity.

9. Conclusions

This review provides information and analysis of published scientific data on eight species of the genus Malachra L. of the family Malvaceae: Malachra alceifolia Jacq., Malachra capitata (L.) L., Malachra fasciata Jacq., Malachra radiata (L.) L., Malachra ruderalis Gürke., Malachra rudis Benth., Malachra helodes Mart., Malachra urens Poit., and Malachra urens Poit. ex Ledeb. & Alderstam. The plants are widely distributed in America, Africa, and Asia, with a greater distribution of species in the tropical and subtropical regions of Colombia and Brazil. These plant species have shown important applications in traditional medicine since their aqueous extracts are used for treating infectious, inflammatory, respiratory, digestive, and neurological problems. The active phytoconstituents isolated from the genus may be useful for the evaluation and identification of molecular targets against infectious pathogens or inflammatory processes. The presence of groups of metabolites such as flavonoids, sterol-terpenoids, and phenolics, including gallic acid, caffeic acid, quercetin, and β-sitosterol compounds may be associated with biological processes with activities such as antidiarrheal, antiepileptic, antiulcerogenic, antioxidant, anticonvulsant, hepatoprotective, antiviral, anticancer, antibacterial, and anthelmintic, with inflammatory activity being the most widespread. In turn, the presence of peptides with pharmacological potential, contribute to the search for drugs against oncological, metabolic, cardiovascular, and neglected tropical diseases. Therefore, this review contributes to the baseline knowledge for the search of information on the validation of the therapeutic use and conservation of traditional and ancestral knowledge of plant biodiversity in America, Africa, and Asia countries, as well as contributes to basic concepts for future research aimed at the discovery of new drugs.

Author Contributions

All authors have written, read, and approved the final version of the manuscript. L.C.-C., H.G.-E., and F.S.-H., were responsible for the first draft of the manuscript; J.S.-H., E.T.-N., J.M.-C., A.E.-G., K.J.A., and E.d.O.-F. participated in the coordination and guidance. All authors have read and agreed to the published version of the manuscript.

Funding

The Program to Support Research Groups, Vice-Rectory for Research at the University of Cartagena (N° 031-2021). This work was supported by the National Program for Doctoral Formation Minciencias (L.C.C: 727-2015, F.S.H: 8852-2020).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

All authors acknowledge the collaboration of Isabella Gonzalez Meza (isacienciag22@gmail.com) who was responsible for preparing the illustrations of the Malachra species.

Conflicts of Interest

The authors declare no conflict of interest.

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