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INTRODUCTION
The Juniperus genus, commonly referred to as “cedars” in English and “enebro” or “sabina” in Spanish, comprises 67 species and 37 varieties (Adams 2014). From Tibetan mountains to tropical islands, juniper trees and shrubs are distributed in all continents except Antarctica. Of the 114 taxa, seven are localized in the Caribbean archipelago: J. gracilior var. gracilior (Pilger), J. gracilior var. ekmanii (Florin) R. P. Adams and J. gracilior var. urbaniana (Pilger et Ekman), endemic to Hispaniola island, J. gracilior var. saxicola (Britton et P. Wilson), endemic to Cuba, J. barbadensis var. barbadensis (Linnaeus), endemic to St. Lucia, J. barbadensis var. lucayana (Britton) R. P. Adams, found in Cuba, Bahamas and Jamaica, and J. bermudiana (Linnaeus), endemic to Bermuda (Adams 2014).
Species within the Juniperus genus have long been used for therapeutic purposes and known for their pharmacological properties (Seca et al. 2015). Their chemical components have also been utilized in food production as flavoring (Falasca et al. 2013) and could be used as food preservatives (Lesjak et al. 2017). Additionally, polyphenols and other compounds of the genre provide an essence potentially used in the cosmetic (Rangel et al. 2018), while also being interesting for pharmaceutical industries, with individual bioactive compounds being potential leads for new drug development (Kwon et al. 2010, Tavares and Seca 2018). Although these investigations have been gathered by review articles such as those written by Seca and Silva (2006), Seca and collaborators (2015) and Tavares and Seca (2018), the economic value and potential of the critically endangered J. gracilior (Pilger) Hispaniolan varieties have not been described (García et al. 2016). This review aims to emphasize the current and potential use of bioactive chemical components from J. gracilior by compiling pertinent information of phylogenetically proximal taxa (J. gracilior var. saxicola, J. barbadensis var. barbadensis, J. barbadensis var. lucayana and J. bermudiana). Information available in Dominican gobernmental reports and overall bibliography was consulted to provide a comprehensive review of J. gracilior chemical components and to highlight its economic potential as a way of guaranteeing this species’ conservation (Newton 2008).
JUNIPERS IN THE HISPANIOLA ISLAND, ENVIRONMENTAL SITUATION AND ECONOMIC IMPORTANCE
The Hispaniola is a Caribbean island comprised of two countries, the Dominican Republic and Haiti. The forest cover of the island is reported to be ~2 % on the west side (Haiti) and ~ 41 % on the east (Dominican Republic) (Posner et al. 2010, MIMARENA 2019). These habitats have a biodiverse flora with an array of endemic species, being especially true in the mountainous territory, which holds pine forests and hundreds of endemic species, including its most representative conifer species Pinus occidentalis (Swartz), Podocarpus hispaniolensis (Laubenfels) and J. gracilior (Posner et al. 2010, Cano-Ortiz et al. 2016, , MIMARENA 2019). The island’s juniper (Juniperus) varieties (figure 1) inhabit elevations between 1,000 and 2,550 meters above sea level, with locations (figure 2) differing among varieties J. gracilior var. gracilior inhabits Dominican mountainous ranges such as Sierra Martín García, Cordillera Central, Sierra de Bahoruco (Zanoni and Mejia 1986) and Sierra de Neiba (Familia et al. 2019), while J. gracilior var. ekmanii is found in the Haitian Massif de la Selle, Massif du Nord (Adams 1983) and the Dominican Sierra de Bahoruco (Adams 2014), and J. gracilior var. urbaniana occupies Haitian Massif de la Selle and Dominican Sierra de Bahoruco (Adams 2014).
Figure 1 Morphology of the three endemic J. gracilior varieties. A) Leaves and berry (purple structure), gracilior variety; B) gracilior variety tree; C) Leaves and cones (yellow structures), ekmanii variety; D) Trunk, ekmanii variety; E) Leaves and cones (yellowish structures) urbaniana variety; F) urbaniana variety shrub. Photo credits: Carolina Juncá (A, B) and Amelia Mateo (C, D, E, F). Morfología de las tres variedades endémicas de J. gracilior. A) Hojas y fruto (estructura morada), variedad gracilior; B) Árbol, variedad gracilior; C) Hojas y conos (estructuras amarillas), variedad ekmanii; D) Tronco, variedad ekmanii; E) Hojas y conos (estructuras amarillas), variedad urbaniana; F) Arbusto, variedad urbaniana. Fotografías tomadas por Carolina Juncá (A, B) y Amelia Mateo (C, D, E, F).
Figure 2 Distribution of J. gracilior in Hispaniola Island. Sightings obtained from GBIF (GBIFab) and field trips organized by the Instituto Tecnológico de Santo Domingo (INTEC) between 2018 and 2019 (unpublished data). Distribución de las variedades de J. gracilior en la isla de la Hispaniola. Avistamientos obtenidos de GBIF (GBIFab) y de viajes de campo organizados por el Instituto Tecnológico de Santo Domingo (INTEC) entre 2018 y 2019 (datos no publicados).
Although these forests represent an environmental and economic benefit for the island, since colonial times, unsustainable depletion of their vegetation has resulted in significant forest reduction and in the critical endangerment of many endemic taxa (Posner et al. 2010, García et al. 2016). The three J. gracilior varieties have been jeopardized due to this anthropic intervention. Mainly, as a result of continuous community and farmland establishment and tree logging, which locals undertake to economically sustain themselves and supply the demand of the fragrant ekmanii and gracilior wood, coveted in the territory (Adams 1983, Peguero and Clase 2015). Since in the 1980s, reforestation efforts have been made on the island, however, the endemic junipers have not taken a significant role in this rehabilitation (Williams 2011, MIMARENA 2019). Two organizations, Dominican National Botanical Garden [2007 - ongoing] and Arche aux Plantes [2013 - 2018], have in recent times, undertaken projects which aim to conserve and propagate seeds of the species (Conservatoire Botanique National de Brest 2017, Mattana et al. 2017). Nevertheless, these have not sufficed to augment populations enough to reduce extinction risk.
BIOACTIVE PREPARATIONS AND EXTRACTS FROM CARIBBEAN JUNIPERS
Juniperus species have been used in traditional or folk medicine even when the scientific bases of their mode of action and the chemicals behind their bioactivity were unknown. Within the genus, J. oxycedrus and J. communis are the most studied in terms of their pharmacological and therapeutic effects (Tavares and Seca 2018). The list of referenced properties pertaining the extracts of their aerial parts is ample, including antifungal (Ortiz et al. 2004), insect repellent (Jacobson 2018), antitussive (Carpenter et al. 2012), antihypertensive (Usmanghani et al. 1997), diuretic (Öztürk et al. 2011), antiseptic (Khare 2007), anti-inflammatory (Khare 2007, Jazayeri et al. 2014), carminative (Usmanghani et al. 1997, Khan et al. 2012) hypoglycemic (Orhan et al. 2012), antioxidant (Jazayeri et al. 2014) and abortive (Öztürk et al. 2011), while also being used as remedies for urinary infection (Grosourdy 1864), cold, bronchitis (Öztürk et al. 2011) diabetes (Orhan et al. 2012, Carpenter et al. 2012), asthma (Khan et al. 2012), urticaria, dysentery, leucorrhea (But et al. 1997), haemorrhoids (Öztürk et al. 2011) and tuberculosis (Omari et al. 2019).
Although a vast array of information can be found for taxa in territories outside the Caribbean, for the four species that do inhabit these islands, historical uses bibliography is scarce. Only J. bermudiana preparations have been reported to be utilized in precolonial times for medicinal and culinary purposes (Wolsak 2017). Nevertheless, studies have reported that Caribbean junipers have been employed in treating urinary infections and have also present cytotoxic, antioxidant, antibacterial and pest repellency properties (Fitzgerald et al. 1957, Grosourdy 1864, Martínez et al. 1996, Jacobson 2018). A list of the bioactivities attributed to Caribbean juniper preparations can be found in table 1.
JUNIPERS AS A SOURCE OF PHYTOCHEMICALS AND BIOACTIVE COMPOUNDS
Besides the interest shown for its bioactive preparations, Juniperus genus has been investigated for phytochemicals such as abietatriene derivatives, widdrol, deoxypodophyllotoxin, amentoflavone, dehydroabietic acid and limonene, whose properties could aid in new drug and product development (Kwon et al. 2010, Seca et al. 2015, Tavares and Seca 2018, Mukhtar et al. 2018). Among these taxa, those form the Caribbean are known to possess potent antitumor molecules against human cancer cell lines. For instance, in these taxa, researchers have been able to identify deoxypodophyllotoxin (Tammami et al. 1977), considered to be one of the most cytotoxic metabolites in the genus (Tavares and Seca 2018), and its biosynthetic product podophyllotoxin (Renouard et al. 2011), whose concentrations in Caribbean taxa have made J. bermudiana its second most important productor (Bazaldúa et al. 2019). Chemical studies have also led to the detection of other useful compounds such as amentoflavone (Gadek and Quinn 1985), a flavonoid with properties such as antitumoral (Chen et al. 2015) antimicrobial (Coulerie et al. 2013), antioxidant (Li et al. 2014), anti-inflammatory (Abdallah et al. 2015), antidiabetic (Laishram et al. 2015) and diuretic (Aguilar et al. 2015, Tavares and Seca 2018). Additionally, widdrol has been found, a lignin reported to be antiproliferative against adenocarcinoma HT29 cells (Kwon et al. 2010), lipolysis inducer in mice adipocytes (Jeong et al. 2015) and inhibitor of B. cinerea growth (Ortiz et al. 2005). Moreover, other compounds with antifungal activity against B. cinerea have been identified and evaluated, including 15-hidroxy-α-pseudowiddrene, cedrol, 3-hydroxypseudowiddran-6(7)-en-4-ol, 12-hydroxywiddrol, sandaracopimaric acid and α-bisabolol (Ortiz et al. 2004, 2005).
Besides the aforementioned compounds, which have been uncovered and bioassayed, other molecules have been reported as part of the essential oil characterization of Caribbean junipers. A list summarizing reported compounds can be found in table 2. Said characterization of foliar terpenes was used to determine the systematic relationship among the taxa utilizing gas chromatography coupled with mass spectrometry (GC-MS) (Adams 1983, 2000). These studies revealed that in Hispaniolan varieties, bornyl acetate accounts for more than 30 % of their essential oil terpene content, followed by terpinen-4-ol, sabinene, limonene in J. gracilior var. gracilior, limonene and sabinene in J. gracilior var. ekmanii, and sabinene, limonene and terpinen-4-ol in J. gracilior var. urbaniana (Adams 1983, 2000). Junipers found in Caribbean territories other than this island do not possess bornyl acetate as their major essential oil component. Perhaps the best example is the Cuban J. gracilior variety, saxicola, which has 4-epi-abietal, elemol and sabinene as its majoritary terpenes, only having 0.3 % bornyl acetate in its oil (Adams 2000). As for the remaining Caribbean junipers: J. barbadensis var. barbadensis has limonene, sabinene, terpinen-4-ol, and α-pinene, while J. bermudiana, has limonene, α-pinene and camphor, and Juniperus barbadensis var. lucayana α-pinene, limonene and sabinene as their major essential oil terpenes (Adams 2000). The bioactive potential of the pure form of some of these majority essential oil compounds can be consulted in table 3.
Table 2 Summary of identified metabolites in Caribbean taxa. Resumen de los metabolitos identificados en taxones caribeños.
+: compound not found in PubChem, structure taken from reference; x: unspecified; *: acetone extraction treated with petroleum ether and benzene;**: a novel compound found in the taxa; CC: column chromatography; TLC: thin layer chromatography; IR: infrared spectroscopy; H-NMR: proton nuclear magnetic resonance; GC: gas chromatography coupled to mass spectrometry; HPLC: high-performance liquid chromatography; MS: mass spectrometry; C-NMR: carbon nuclear magnetic resonance; UV: ultraviolet spectroscopy; 2D NMR: two-dimensional nuclear magnetic resonance spectroscopy.
Table 3 Essential oil majority terpenes of Hispaniolian junipers and their pure form bioactivities. Bioactividades de las formas puras de los terpenoides mayoritarios en el aceite esencial de los Juniperus de la Hispaniola.
In general, literature describing the chemical composition and usage of the Caribbean taxa is concentrated on J. bermudiana and J. barbadensis var. lucayana (Fitzgerald et al. 1957, Tammami et al. 1977, Gadek and Quinn 1985, Khan 1989, Martínez 1996, Ortiz et al. 2004, 2005, Nuñez et al. 2007, Renouard et al. 2011, Wolsak 2017). The other taxa are only mentioned in studies about insect repellency and are not reported for their traditional usage and medicine bibliography of their respective countries (Jacobson 2018). Studies involving a holistic chemical characterization of these taxa with subsequent bioactivity assays need to be conducted to elucidate the phytochemical composition and potential usage of these conifers. The mentioned pure form bioactivities of these essential oil terpenes, although not accouting for their synergistic or antagonistic interactions with other compounds, might present a lead for future bioactivity assays of the taxa.
FUTURE DIRECTION IN INVESTIGATING JUNIPERS PHYTOCHEMICALS, THE METABOLOMICS APPROACH
As mentioned above, the full phytochemical composition of endemic Caribbean Juniperus spp. is widely understudied. This information, being of pivotal importance for botanical, conservation, and pharmacological purposes, is crucial for bioprospecting studies of the species to increase its protection locally. Currently, among the characterization of living organisms, metabolomics is playing a key role, either alone or in combination with guided biological activity assays (Wishart 2016). Metabolomics is the systematic study, identification and quantification, of the metabolites in an organism a specific moment in time (metabolome) (Tugizimana et al. 2013). And while phylogenetic lineages can help select new taxon targets for bioactivity studies, metabolomics can help identify structurally related metabolites conserved throughout evolution that might be of interest to the investigator (Mawalagedera et al. 2019).
In a broad sense, the steps of a metabolomics study (figure 3) are as follows: material sampling and extraction, extract analyses or data acquisition, statistical analyses and metabolite identification (Choi and Verpoorte 2014). How these steps are performed ultimately depends on the investigator’s objective and approach (targeted or untargeted). A targeted approach identifies and quantifies a few known and predetermined metabolites, while an untargeted one aims to study all the known and unknown metabolites present in a sample (Tugizimana et al. 2013).
Figure 3 General metabolomics workflow. Flujo de trabajo general para un experimento de metabolómica.
For metabolite identification and quantification, different extraction solvents and methodologies can be employed. According to the analytical platform used, metabolomic studies mainly belong to two groups, MS- and RMN- based. These can be utilized in parallel or combination to other classic protocols of thin layer, liquid or gas chromatography, spectrometry and spectroscopy (Nuñez et al. 2007). The platforms employed in the identification of chemical components of the Juniperus Caribbean clade can be found in table 2. As a whole, this genus has had compounds from leaf, wood and berry extract characterized, with most of these investigations being designed with a targeted approach to specific chemical groups (Adams 2000, Renouard et al. 2011, Falasca et al. 2013, Rangel et al. 2018). For the identification of novel and/or useful bioactive compounds of J. gracilior and other Caribbean junipers, an untargeted approach focused on a larger range of metabolites including uninvestigated chemical groups such as polyphenols, known antioxidants, anti-mutagenic and antitumor compounds (Rangel et al. 2018), might need to be used.
