The phytochemistry and ethnobotany of the 3 southern ... · PDF filesouthern African genus Eucomis (Hyacinthaceae: Hyacinthoideae) ... Phytochemistry and ethnobotany of the genus Eucomis

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Phytochemistry: Advances in Research, 2006: 69-85 ISBN: 81-308-0034-9 Editor: Filippo Imperato

3 The phytochemistry and ethnobotany of the southern African genus Eucomis (Hyacinthaceae: Hyacinthoideae)

Chantal Koorbanally1, Neil R. Crouch1,2 and Dulcie A. Mulholland1 1Natural Products Research Group, School of Chemistry, University of KwaZulu-Natal, 4041, Durban, South Africa; 2Ethnobotany Unit, South African National Biodiversity Institute, P.O. Box 52099, Berea Road, 4007, Durban South Africa

Abstract The endemic African genus Eucomis (Hyacinthaceae) has long been one of the most highly regarded sources of ethnomedicines in southern Africa, attracting the attentions of toxicologists, pharmacologists and phytochemists. This chapter reviews the ethnobotany of this small group of fourteen described taxa (ten species), and the known phytochemistry. Six taxa (five species) have been recorded used traditionally, for

Correspondence/Reprint request: Dr. Dulcie A. Mulholland, Natural Products Research Group, School of Chemistry, University of KwaZulu-Natal, 4041, Durban, South Africa. E-mail: [email protected]

Chantal Koorbanally et al. 70

ailments largely related to inflammation and pain, and conditions as diverse as urinary diseases, colic, hangovers, syphilis, fractures, backache, rheumatism and teething. A total of six species have been phytochemically investigated, resulting in the isolation of thirty-nine constituents. These include four classes of homoisoflavonoids, as well as benzopyranones, spirocyclic nortriterpenoids, acids, a saponin glycoside and a chromanone. The sources, structures and spectral data of these isolates are here detailed. Introduction The near-cosmopolitan family Hyacinthaceae Batsch ex Borckh. is well represented in southern Africa by one of two main centres of diversity, harbouring approximately half of the world’s representatives. This is in three Old World subfamilies, the Hyacinthoideae, Urgineoideae and Ornithogaloideae. Amongst these are several endemic and near-endemic genera, including the small but horticulturally and ethnomedicinally important genus Eucomis L’Hér., the pineapple lilies. This review considers the phytochemistry and ethnobotany of Eucomis, in view of its reported toxicity, popularity in ethnomedicine and potential as a source of non-steroidal anti-inflammatory drugs. Geographic and taxonomic considerations Eight of the ten Eucomis species (with fourteen described taxa) are found only in southern Africa, with E. zambesiaca Bak. and the typical subspecies of E. autumnalis (Mill.) Chitt. extending north of the Limpopo River into south tropical Africa [1]. A possible fifteenth taxon, as yet undescribed, is localised in southeastern Lesotho [2]. A treatment of each species has been provided by Compton [3] who arranged his overview by growth, environmental parameters and distinguishing features. Within the Flora of Southern Africa (FSA) region the subfamily Hyacinthoideae is represented by two tribes, the newly circumscribed Pseudoprospereae [1], and the long-established Massonieae Bak. to which Eucomis is assigned. Whereas overall family taxonomy is in remarkably contentious flux [1,4,5], both molecular and morphological characters concur in circumscribing Eucomis L’Hér. Accordingly, the genus size and nomenclature has not altered substantially in recent years, save for the recognition of E. pole-evansii N.E.Br. as a larger, more northerly subspecies of E. pallidiflora Bak [1]. Eucomis is readily recognisable in the field in possessing a prominent coma or set of leaf-like bracts atop the many-flowered cylindrical racemes. This character of the flower cluster has led to their common name “pineapple lilies”. At the base of the inflorescence, several synanthous strap-shaped or obovate leaves are present in a rosette. As deciduous perennials, they possess papery bulbs that are usually subterranean, and conical or globose in shape. Although representatives of the tribe Massonieae

Phytochemistry and ethnobotany of the genus Eucomis 71

are distributed widely in both summer and winter-rainfall regions, Eucomis is found primarily in the summer-rainfall zone where it is a characteristic component of moist grasslands in montane and subalpine areas. Only E. regia (L.) L’Hér. is localised in the winter-rainfall region, where it inhabits arid, shady sites, in Namaqualand and the Karoo. Although all pineapple lilies are similar in floral morphology, plant habitat, stature and differences in the purple colouration of leaves and flowers delimit the species boundaries. The ethnobotany of Eucomis has been fairly well documented. It should be noted though that ethnobotanical and other data reported prior to 1976 for E. regia (syn. E. nana (Burm.f.) L’Hér.) from Lesotho, KwaZulu-Natal and the Eastern Cape are arguably relevant instead to the most recently described genus member, E. schijffii Reyneke [6]. A fair amount of confusion is still perpetuated in recent texts in this regard [7], further misinterpretation entering on account of confusion between E. regia and E. autumnalis (Mill.) Chitt. subsp. clavata (Bak.) Reyneke in the literature [8].

Ethnomedicinal usage The Hyacinthaceae ranks as one of the most important families in ethnomedicine along the eastern seaboard of southern Africa [9,10]. A recent survey revealed that of the most important species marketed by Durban street traders, seven hyacinthacs occurred within the top seventy, with three of these (Merwilla plumbea (Lindl.) Speta [syn. Scilla natalensis Planch.], E. autumnalis and Bowiea volubilis Harv. ex Hook.f.) ranked in the top ten [9]. An earlier trade report [11] recorded E. autumnalis as the second most heavily traded species amongst herb traders in KwaZulu-Natal, and E. bicolor Bak. as the 30th so. Eucomis comosa (Houtt.) Wehrh. has been noted in the ethnomedicinal plant trade both in the Eastern Cape Province (known as umphompho) [12] and to the north in Durban, KwaZulu-Natal [10], and E. bicolor in both Durban [10] and Johannesburg [13]. Traditional ethnomedical usage of Eucomis subjects is presented in Table 1.

Toxicity Of the three subfamilies in southern Africa, the Hyacinthoideae is considered the least poisonous generally, with some taxa even being locally identified as edible [14]. Links between human deaths attributed to homicidal agents and to ethnomedicinal preparations comprising hyacinthaceous elements have been well established [15]. However, this is generally attributable to bufadienolide-containing urgineoid taxa such as B. volubilis [15,16,17] although overdosing on preparations of hyacinthoid taxa such as E. autumnalis and E. comosa is not unknown [15,18]. A survey of the toxicity of the whole family has earlier been published [19] including an account of


Eucomis feeding trials undertaken by the Onderstepoort Veterinary Research Institute near Pretoria [20]. During these experiments sheep drenched with fresh bulbs of E. autumnalis (as E. undulata Ait.) presented with listlessness, anorexia, foaming at the mouth, tympanites, an inactive rumen and a strong pulse. Death occurred within twenty-four hours; post-mortems revealed severe ascites, hydropericardium, oedema and emphysema of the lungs, hyperoemia of and regressive changes in the liver and kidneys [20]. This same species has been identified as potentially fatal to man if ingested in large quantities [21,22], the main features of poisoning being diarrhoea, abdominal pain and renal failure [15]. Eucomis comosa is also considered potentially toxic by some researchers [23]. Internal administration of this plant is said to frequently produce a rash [15]. A haemolytic saponin (glucoside) has been isolated from the bulb of E. autumnalis, which when intravenously injected into experimental animals resulted in death by respiratory paralysis [24]. The saponin(s) present in the bulb have historically been employed by the Southern Sotho as a soap [25], even though the sap is reportedly irritant to the hands [26]. Bioactivity and ethnopharmacology The pharmacological value of constituents isolated from this genus is still insufficiently known. Several reports on the biological activity of homoisoflavonoids indicate their anti-inflammatory, antibacterial, antihistaminic, antimutagenic and angioprotective qualities, and value as potent phosphodiesterase inhibitors [27,28,29]. Antibacterial activity (in bioautographic and microplate assays) against Staphylococcus aureus has been demonstrated for four homoisoflavonoids isolated from E. comosa and one from E. humilis Bak. [30]. The widespread cross-cultural use of bulbs to treat disorders marked by inflammation and attended by pain (e.g. rheumatism)(Table 1) suggests true efficacy and hence a rational basis for the selection of pineapple lily species as ethnomedicinals. Accordingly, three homoisoflavonoids isolated from separate Eucomis species (E. pallidiflora Bak. subsp. pole-evansii (N.E.Br.) Reyneke ex J.C.Manning, E. comosa and E. humilis) were screened for anti-inflammatory activity, using indomethacin as a standard [31]. The inhibition of prostaglandin synthesis in microsomal cells was evaluated followed by screening for specific inhibition of cyclooxygenase enzymes (COX-1 and COX-2). None of the above Eucomis-sourced homoisoflavanones showed even moderate anti-inflammatory activity based on, particularly, COX-1 inhibition, nor was significant anti-inflammatory activity observed when inhibition of prostaglandin synthesis in microsomal cells was considered [31]. Notably, despite earlier work [32] that has revealed the significant inhibition of COX-1 and COX-2 enzymes by extracts of the bulbs of E. humilis, E. pallidiflora subsp. pole-evansii and E. comosa, isolates from all three species showed only low activity in the same assays [31]. Accordingly, data obtained from these


compound-specific investigations does not confirm homoisoflavonoid presence as the basis for the ethno-selection of Eucomis to treat a variety of pain and inflammation-related ailments. The species most popularly used traditionally as an anti-inflammatory, E. autumnalis (Table 1) has been the subject of a number of studies prospecting

Table 1. Ethnomedicinal uses of Eucomis species, with constituents isolated.


Table 1. Continued

for non-steroidal anti-inflammatory drug (NSAID) leads [33,34,35]. Aqueous and ethanolic extracts of bulbs of E. autumnalis inhibited prostaglandin-synthesis 73% and 90% respectively, relative to indomethacin (0.5 µg) at 66.5% [33]. Leaf extracts showed significantly lower anti-inflammatory activity (COX-1 assay) than those of bulbs [36]; the TLC profile of extracts indicated that major constituents varied with plant part [36]. The selective COX-2 activity (indicated by lower COX-2/COX-1 ratios) of bulb extracts relative to that of leaves has been cited [35] as further validation of the traditional use of bulbous material. Of six lanosterol oligosaccharides isolated from E. bicolor, only one showed significant activity in a primary screen for antitumour-promoting compounds [37]. This eucosterol glycoside (at 50 µgml-1) caused 44% inhibition of TPA-stimulated 32P incorporation into phospholipids of HeLa cells. The activity of such lanosterol oligosaccharides may relate to the use by the Tswana and Pedi to respectively relieve abdominal distensions and abdominal pain using bulb decoctions of E. autumnalis [15].

The chemistry of Eucomis The subjects of this overview, with common synonyms, are listed in Table 1. From the taxa represented, four classes of homoisoflavanones have been isolated, as well as benzopyranones, spirocyclic nortriterpenoids, acids, a saponin glycoside and a chromanone. Structural data for compounds are provided (Table 2), as are spectral data and plant sources (Table 3). Many of the thirty-nine Eucomis constituents so far isolated (Table 2) have been found in other Hyacinthoideae genera [19], and several compounds are common to


more than one Eucomis taxon (Table 3). Following the characterization of the remaining eight or nine taxa, it would be interesting to consider the chemotaxonomic significance of findings. Of the fourteen Eucomis taxa so far described, only six have been phytochemically profiled. Eight natural taxa (representing seven species) remain to be investigated: E. autumnalis subsp. amaryllidifolia, E. autumnalis subsp. clavata, E. comosa var. striata, E. pallidiflora subsp. pallidiflora, E. regia, E.humilis, E. vandermerwei and E. zambesiaca. 2.1 Dibenzo-α-pyrones The isolation of these compounds from E. autumnalis have been questioned in the light of the isolation of the isomeric methylxanthones from the closely related genus Drimiopsis Lindl. & Paxton [48]. These benzopyranones have not been isolated from any other species within the Hyacinthaceae. Two collections of E. autumnalis are currently being investigated in our laboratories to confirm the structures of these isolates.

Table 2. Phytochemical constituents of the genus Eucomis.

2.2 Homoisoflavonoids Homoisoflavanoids (commonly known as homoisoflavanones or 3-benzyl-4-chromanones) are a small group of compounds whose occurrence has thus far been restricted largely to the Hyacinthaceae. Homoisoflavonoids were first reported in 1967 from the genus Eucomis [50]. They are known to be concentrated in the waxy, scale like layers of the bulbs [29]. Four different classes of homoisoflavonoids have been isolated from Eucomis.


2.2.1 3-Benzyl-4-chromanone This class of homoisoflavonoid consists of a sixteen carbon skeleton with

a chromanone moiety to which is attached a benzyl group at the 3-position. This is the commonest class of homoisoflavonoid.

2.2.2 3-Hydroxy-3-benzyl-4-chromanones This class of homoisoflavonoid differs from the 3-benzyl-4-chromanones in that they have a hydroxyl group at the 3-position. The 3-hydroxy-3-benzyl-4-chromanones generally occur as a mixture of C-3 epimers.


2.2.3 3-Benzylidene-4-chromanone This class of homoisoflavonoid has a double bond or a benzylidene moiety attached at the 3-position. The orientation about the double bond can be either cis (Z) or trans (E).


2.2.4 Scillascillin-type homoisoflavonoid This is a rare class of homoisoflavonoid whereby a fourth 3-spirocyclobutene ring is present. The extra four-membered ring compounds are referred to as scillascillin-type compounds. Circular dichroism experiments have shown the absolute configuration at C-3 to be (R).

2.3 Spirocyclic nortriterpenoids The spirocyclic nortriterpenoids are characterized by a basic lanosterol triterpenoid skeleton with the loss of one of the terminal methyl groups of the side chain. Compounds 29-34 are lanosterol oligosaccharides with aglycone skeletons that are closely related to eucosterol (27). Compound 36, is also a lanosterol oligosaccharide with a modified side chain forming a spiro-lactone group.



2.4 Other triterpenoid derivatives

2.5 Aromatic compounds


Table 3. References to the Eucomis source, phytochemical constituents and their spectroscopic data.


Table 3. Continued

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The phytochemistry and ethnobotany of the 3 southern ... · PDF filesouthern African genus Eucomis (Hyacinthaceae: Hyacinthoideae) ... Phytochemistry and ethnobotany of the genus Eucomis