Wednesday, December 3, 2014

Frankincense- Origins and Medical Research

Title: The Burseraceae Family of Flowering Plants
Author: Jillian Vaught

The Burseraceae family of flowering plants is of the order Sapindales (“Burseraceae”). Sources report the Burseraceae family to be composed of at least 16 genera: Aucoumea, Canarium , Crepidospermum, Dacryodes, Elaphrium, Garguga, Haplolobus, Protium, Santiria, Tetragastris, Tingulonga, Trattinnickia, and the four well known genera: Beiselia, Boswellia, Bursera, and Commiphora. The Plant List, a working list of the known plant species maintained by efforts of Missouri Botanical Gardens, Kew, and Royal Botanical Gardens, encompasses 1,870 scientific names of species rank for the Burseraceae family. Of the 1,870 species rank names, 615 are accepted names of species (Burseraceae, The Plant List) (Figure 1-1). The Burseraceae family is a monophyletic group, confirmed by molecular data. (Daly, 2011)

Studies by the Word Pollen and Spore Flora have worked to incorporate pollen morphology of Burseraceae into the classification of three tribes: Protieae, Bursereae, and Canarieae. Within these three tribes, the morphology of the pollen grain is being used to classify the tribes by pollen type. Pollen type is delimited by grain polarity, polar outline, length of polar axis, width of equatorial axis, shape, exine type, exine surface, apocolpial wall thickness, apocolpial ultrastructure, and the presence or absence of apocolpial endexine. From these data (Harley, Song, Banks, 2005), 14 pollen types have been distinguished. Of the 14 types, 9 are unique to Burseraceae. Seven of the uncommon pollen types are represented by only one taxon and three of these taxa represent monospecific genera. DNA data has also been used to support the pollen morphology that Bursera and Commiphora share a close relationship as well as Garuga and Boswellia. At this time, most of the pollen grain types are limited to Burseraceae of the tribe Protieae. Pollen grain types for the tribes Bursereae and Canarieae have not been published (Harley, Song, and Banks, 2005).

The Burseraceae family is commonly called the Torchwood family or Incense family for their aromatic sap or resin. Of the 16 genera, Commiphora is the largest genus encompassing nearly 200 species. Commiphora is most commonly recognized as the "Myrrh" genus, while Boswellia is recognized as the "Frankincense" genus. The genus Bursera is economically important for its reddish-brown wood (Dimmitt, 2014). Its economic importance makes it key to investigation by ecologists who endeavor to preserve biological habitats from consumption. Ecologists working with Burseraceae commonly encounter taxonomic challenges. Molecular and phylogenetic analysis shows Bursera and Commiphora to be closely related. In this regard, placing species between the two genuses has been reason for debate especially in the case of South American species C. leptophloeos. By pollen morphology and geographic location, C. leptophloeos is placed in the Commiphora genus; however, new molecular data suggests it is most closely related to Bursera. Taxonomic difficulties such as this are commonly encountered within the Burseraceae family as molecular data becomes increasingly available (Rosell and Olson, 2010).

A few genera, such as Bursera, have been separated into subclades. Bursera has four major subclades: Simaruba, Microphylla, Fragilis, and Fagaroides. Species are subject to rearrangement within the subclades especially within the Fagaroides where morphological divisions are inconsistent (Rosell and Olson, 2010).

The crown group of the Burseraceae is dated 58 million years ago (Presl). Bursera and Commiphora diverged somewhere between 120 and 60 million years ago and the Commiphora did not completely diversify until some 32 to 23 million years ago. It is believed that the varying distribution of these two genera is due to continental drift (Presl).

Phylogenies place the Burseraceae and Anacardiaceae as sister clades within the Sapindales. Beiselia is a recently-investigated family that is likely sister to the Burseraceae, having many sister automorphic features (Daly, 2011). Interestingly, the Burseraceae family has consistently been placed in the same order as Meliaceae, Rutaceae, and Simaroubaceae in different systematic placements (Harley, Song, and Banks, 2005).

Weeks and Simpson (2007) tested the monophyly of Commiphora to hypothesize the events of its diversification and widespread geography. Using fossil calibrations, they were able to hypothesize that the success of this tree was due to post-Paleogene aridification that selected for this dry-adapted species. Evidence from fossils shows that dry-adapted tropical floras like Commiphora were already present in Africa prior to the Paleogene; however, their species expanded most likely as a result of the post-Paleogene climate. Dry-arid climate must hold a key to the diversity of Commiphora considering approximately 150 of its 190 species can be found throughout desert and seasonally dry habitats (Weeks and Simpson, 2007).

Weeks (2005) previously determined that Commiphora was a sister to a subgenus of American Bursera species. Fossil calibrations, DNA analysis of intergenic spacers, and Bayesian inference from Weeks and Simpson’s analysis suggests that Commiphora is sister to Paleo-tropical Bursera tonkinesis, not the American Bursera clade. Further publications on this subject may be able to support the listing of Bursera as an exclusively American taxon. This new phylogenetic information and genera age via fossil calibrations of B. tonkinesis are evidence for intercontinental transfer of Burseraceae from North America to Asia while its genus Commiphora spread westward to Africa (Weeks and Simpson, 2007).

Sets of molecular data attained during Weeks and Simpson’s analysis were used to determine the probability of relationships among three Burseraceae genera. Nuclear and chloroplasts data sets were used to assemble maximum parsimony trees for Commiphora, Bursera, and Elaphrium. Age calibration from fossil-based evidence formed nodes in the trees. The resulting 100 trees were scored with maximum parsimony, compiling the average age and confidence for each node. All species were scored based on their presence in the following regions: Africa, Madagascar, India, southeast Asia, South America, Mexico, and North America. The results showed that the Commiphora species monophyly was supported by 100% parsimony bootstrap support and 100% Bayesian posterior probability. The sister relationship of Commiphora to Paleotropical B. tonkinensis is 53% parsimony bootstrap support and 94% Bayesian posterior probability. Both parsimony bootstrap support and Bayesian posterior probability highly support the sister relationship of Elaphrium, B. tonkinensis, and Commiphora (Weeks and Simpson, 2007).

Morphological Characteristics
The Burseraceae family includes trees or shrubs, all of which have resin ducts within the bark containing triterpenoid compounds and aromatic oils. The Burseraceae are mostly dioecious. The leaves are alternate or pinnately compound. The inflorescences are usually axillary, rarely terminal, with paniculate or uniflorous arrangements. The flowers are actinomorphic having 3-5 sepals which are connate and form a tube at the base. They may have 3-5 petals that are either free or adnate to the calyx. The stamens are in 1-2 whorls (equaling or twice the number of petals). The filaments originate outside the nectar-discs (Salywon, 1999). The ovaries are superior with about 3 locules, and there are usually 2 ovules per locule. The stigmas are 2-5 lobed. They produce drupe fruits, with mostly dry mesocarp and 1-5 stoney seeds. The fruits are generally dehiscent with 2-5 valves (Woodson and Porter, 1970). The seeds commonly have a pseudoaril and always lack endosperm (Salywon, 1999).
Figure 3-1 shows Burseraceae of the species Bursera tomentosa. Bursera is categorized by tree or shrubs with smooth or rough bark. Thin sheets peel off of the older bark or in thick scales. The leaves are odd-pinnate or bi-pinnate. The leaf margins are entire to toothed. Inflorescences appear in axillary raceme panicles, which usually develop just before the new leaves. The flowers are usually small and unisexual with 3-5 white or yellowish petals that extend beyond the sepals. The gynoecium has 2-3 carpels and the ovary is 2-3 lobed. The endocarp is usually one-seeded with no endosperm (Woodson and Porter, 1970).

The genus Protium can be distinguished by larger leaves of entire leaf margins. The inflorescences contain flowers of 4-5 free petals that are usually fleshy with 8-10 stamens. The gynoecium has 4-5 carpels and ovaries of 4-5 lobes. The fruit is globose, ellipsoid, or ovoid with a fleshy and resinous mesocarp (Woodson and Porter, 1970). Protium panamense can be seen in Figure 3-2.

Of the three most economically important genera to be described, Commiphora has one of the most diverse species populations. It can be a tree or shrub with smooth bark of various colors that are found to peel easily. The inflorescence are either paniculate or solitary and in clusters with 4 greenish to yellow petals. Ovaries are made of 3 locules with 2 ovules in each. The drupe fruit produces a single stone and seed (Eggi, 2002). Figure 3-3 shows Commiphora campestris.

Plant Geography
The Burseraceae family is most widespread in tropical America, northwest Africa, and Malaysia. Four genera are known to grow in Panama: Bursera, Protium, Tetragastris, and Trattinnickia (Woodson and Porter, 1970). Commiphora grow ideally in arid zones across sub-Saharan Africa, dominating over 1.6 million square kilometers of the Acacia-Commiphora woodlands in East Africa (Weeks and Simpson, 2007). Commiphora’s major distribution is over Africa, Madagascar, India, and South America. Evidence by fossil calibration and molecular phylogenies suggests that Bursera and Commiphora spread from west to east across Laurasia through the North Atlantic boreotropical corridor. Figure 4-1 shows a Commiphora myrrha tree in the arid North African Sahara. Evidence also suggests that Bursera tonkinensis was transferred from North America to Asia and expanded westward through Africa (Weeks and Simpsons, 2007). Figure 4-2 shows the occurrence of Burseraceae across the world.

The Protieae are found primarily in South America, while the Canarieae tribe are found primarily in Malesia (Harley, Song, and Banks, 2005). Cultivators have found that Arizona provides sufficient arid climate to grow Bursera fagaroides var. elongata and Bursera microphylla (Salywon, 1999). The popular Frankincense genera Boswellia, includes species of Boswellia sacra which are known for their essential oil distilleries in Oman and Yemen. Boswellia carteri from Somalia and Boswellia serrate from India and China are also common frankincense resinous trees (Suhail and Wu, 2011).

Historical biogeographers take into account the effects of global cooling during the Miocene period and how it may have forced tropical species of Commiphora to migrate toward the equator into their current disjunct distribution in Africa and the southeast Asian tropics. In the case of the endemic Malagasy species of Commiphora, biologists find that they comprise more than two unrelated clades and must result from two introductions of the species (Weeks and Simpson, 2007).

Economic Importance
The economic importance of the Burseraceae family extends across the globe from Asia to Africa and back to the United States. The red-barked Gumbo-Limbo tree (Bursera simaruba), residing in south Florida, produces lightweight wood that is great for carving. Before molded plastic, B. simaruba wood was used to make carousel horses (Gilman and Watson, 2006). The wood is still popular for making fishing boats and its fragrant resin is used as incense (“Burseraceae”).

On the west coast of Africa, the Gabonese Republic commercially grows Aucoumea klaineana. A. klaineana is a medium to large evergreen tree with a diameter anywhere from 30-40 centimeters reaching up to 60 meters tall. This tree makes up 90 percent of Gabon’s timber production (“Okoume Fact File”, 2013).

The fruit of Drakryodes edulis is commonly traded between Cameroon, Nigeria, and Gabon. The tree prefers humid lowlands such as those found abundantly in Cameroon. These trees are grown in tree-farmed areas and have great potential as an export, as the trees produce a high yield of fruit each year (Ayuk, Duguma, Franzel, and Kengue, 1999). The fruit is known as “butterfruit” due to its butter-like pulpy oil. The oil of these fruits has attracted western dietary attention for its unsaturated oil, high amino acid content, and minerals like potassium, calcium, and magnesium (Kane, 2010). Figure 5-1 shows a basket of “butterfruit” from Cameroon.

Despite Burseraceae’s use from its pure biomass, its most sought-after family members may be those of Commiphora and Boswellia. The several known species of Boswellia produce what we commonly call frankincense, the essential oil extracted from the tree’s oleo-gum resin. (“Burseraceae”) Not only does the extracted frankincense essential oil show fascinating medical properties, it is sanctioned as a biblical oil. The resin from Commiphora is used to make myrrh, another biblical oil of medical importance (“Burseraceae”).

Biological Information
The flowers of Burseraceae are mostly dioecious. The genera Boswellia, Garuga, Dacryodes, and Bursera all have perfect flowers. Commiphora monoica is one of the rare species that is monoecious. Commiphora samharensis is one of the few speices that undergoes pollination through selfing (Kubitzki, 2011). Members of the Protium spruceanum in Central Brazil produce abundant nectar as a pollination reward. On average, the nectar has a 30% concentration of sucrose (Kubitzki, 2011). Small insects pollinate most of the Burseraceae flowers (Kubitzki, 2011).

The family’s most characteristic trait is the consistency of its oleoresin. The resin contains terpenoids, a class of organic chemicals with a varying 5-carbon skeleton (Maimone). The resin is a mixture of volatile and non-volatile terpene chemical compounds that are most commonly non-volatile in Burseraceae. Biochemists have determined that the family uses terpenoids as a means of attracting pollinators while its toxicity repels herbivores (Kubitzki, 2011).

Further investigation into the chemical compounds that make up the essential oil of the Boswellia genus, shows the isolation of β and α boswellic acid from commercial frankincense resin.  Boswellic acid is a lupine-type triterpene, a structure that has been determined using chemical and spectral evidence such as mass spectrometric techniques. Figure 6-1 shows the structure of β and α boswellic acid. The four main producing species of this resin are Boswellia carteri, Boswellia frereana, B. sacra, and B. serrate. This acid has only been isolated from frankincense, or the Boswellia genus. The isolated contents of boswellic acid appear as a colorless crystal. Since the acid is confined to Boswellia, it has been used to identify archaeological samples of frankincense (Culioli, Mathe, and Archier, 2003).

Frankincense in Medical Research
Frankincense has been highly valued as a component of alternative medicine practice for centuries. Most of the frankincense that is traded internationally is distilled into an essential oil and is from Oman, Yemen, and Somalia (Yousef, 2011). Recently it has sparked the attention of scientific research for its anti-inflammatory and anti-neoplastic effects (Suhail and Wu, 2011). In 2011, research conducted by the University of Oklahoma Health Science Center in Oklahoma City has found the optimal conditions under which the essential oil of Boswellia sacra induces tumor cell-specific cytotoxicity. In their research, Urologists and Physiologist of the university assayed the apoptosis by genomic DNA fragmentation. They then used Western blotting methods to study the oil-regulated proteins of Boswellia sacra’s essential oil that were involved in apoptosis. The results were undisputable, essential oil hydrodistilled at temperatures around 100° C had the greatest response inducing tumor cell cytotoxicity. These oils distilled at high temperature also contained the highest molecular weight of boswellic acid. The research shows that components of the essential oil target and induce cell death in malignant cells. Ongoing research strives to produce an essential oil of Boswellia sacra with consistent chemical composition that can be used for pre-clinical validation of boswellic acid as a cancer fighting agent (Suhail and Wu, 2011).

Youself (2011) published his findings on the effect of distilled frankincense extracts given orally to forty male Wister Albino rates. The experiment shows that after the rats had received frankincense in their water for 30 days, they showed toxic levels of uric acid in the blood. The high levels of uric acid the in blood caused a break down of purine bases in the DNA. In addition, there was an accumulation of creatinine in the kidney and increased levels of nitric acid that stimulated free radicals in the surrounding kidney tissue. The biochemical and histological examination of rats exposed to frankincense concluded that frankincense, as traditional medicine, must certainly be used with precaution (Yousef, 2011).
From timber to medicine, the importance of the Burseraceae family is exceptional. Its confirmed presence on five continents makes it ideal for taxonomic and molecular phylogenetic research. Its trees and shrubs of papery bark appear in the most uncanny arid climate. The family’s consistent production of oleoresin from its bark has survived ancient biblical history and is still being distilled into essential oils in the Middle East. As an alternative medicine and a source of nutrition, members of the Burseraceae family continue to support our developing world into the 21st century.

Figure 1-1 Accepted Species Names from The Plant List (“Burseraceae”, The Plant List)
The status of the 1,870 species names for the family Burseraceae recorded in The Plant List, are as follows:


Figure 3-1 Bursera tomentosa (Woodson and Porter, 1970)

Figure 3-2  Protium panamense (Woodson and Porter, 1970)    

Figure 3-3 Commiphora campestris (Woodson and Porter, 1970)    

Figure 4-1 Commiphora myrrha tree in North African Sahara. (“Prelude Medicinal Plants Database”)

Figure 4-2 The Occurrence of Commiphora across the Globe (Presl)

Figure 5-1 The “Butterfruit” of Drakryodes edulis from Cameroon (Asaah, 2002)

Figure 6-1 a) Structure of β Boswellic Acid. (Culioli, Mathe, and Archier, 2003)

Figure 6-1 b) α Boswellic Acid. (Culioli, Mathe, and Archier, 2003)

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