Illicium

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Illicium

Description

Shrubs or small to medium sized trees, evergreen, glabrous, aromatic with scattered ethereal oil cells. Leaves simple, entire, alternately arranged although often clustered to give appearance of whorls of 3-6 at distal nodes, exstipulate; lamina ovate to elliptic, papyraceous or coriaceous, pinnate venation, apex generally acuminate, base generally attenuate, decurrent; stomata on abaxial surface only, mesogenous, generally paracytic; petioles with groove on adaxial surface. Flowers solitary or in clusters of 2 or 3, mostly axillary, sometimes cauliflorous, bisexual, regular, hypogynous, 1-1.5 cm diam.; pedicels 0.5-7(-10) cm long. Fruit a follicetum of single-seeded follicles, star-shaped, 2-3 cm across, green (ripening red), splitting along ventral edge of each segment when ripe. Seeds solitary in each segment, glossy, brown, with copious oily endosperm.

Distribution

Asia-Temperate: Asia-Tropical:, Borneo (Sabahpresent, Sarawakpresent); Malaya (Peninsular Malaysiapresent) Assam to the Philippines: present Luzon: present Mindoro: present Northern America: Southern America: northern and central Sumatra: present south-eastern North America: present southern Japan to the Malay Peninsula: present
A medium sized genus, with a disjunct distribution in south-eastern North America, Mexico and the West Indies (5 species) and eastern Asia (centre of diversity, with about 35 species). The Asian distribution extends from southern Japan to the Malay Peninsula, and from Assam to the Philippines. In Malesia 1 species: northern and central Sumatra, Malay Peninsula, Borneo (Sabah and Sarawak, with two records from Kalimantan) , and the Philippines (Mindoro and Luzon).

Ecology

Vegetative growth is markedly discontinuous, with periods of dormancy of vegetative buds alternating with active growth (Ng 1973). The resumption of growth involves the rapid elongation of buds to produce stems several centimetres long, which bear small caducous leaves; apical 'pseudowhorls' of leaves are then produced, consisting of alternately arranged normal leaves that are tightly clustered together.

Studies of the reproductive biology of the North American species /. floridanum Ellis and I. parviflorum Michx. ex Vent, have shown that they are pollinated by a wide variety of small insects, but primarily Diptera, with unspecialised feeding habits (Thien et al. 1983; White & Thien 1985). The plants typically grow in very dense populations and produce large numbers of flowers over a short period of time; the inefficiency of the insects in dispersing pollen, however, is suggested as one of the reasons for the typically low seed set. It has also been shown that a gametophytic self-incompatibility mechanism operates, and that the species frequently reproduce asexually by root suckers and runners (Thien et al. 1983; White & Thien 1985).

A system of ballistic seed dispersal (autochory) is apparent in /. floridanum (Roberts & Haynes 1983), although its efficacy in Malesian species has not been demonstrated. Seeds are expelled from the follicle as a result of hygroscopic tensions that develop in the succulent mesocarp walls and possibly also the sclerenchymatous endocarp. The role of water in the dispersal of seeds is unclear: whilst Thien et al. (1983) claim that the seeds can remain afloat for up to 10 days as a result of surface tension and the entrapment of air in an indentation of the testa at the point of attachment of the seed, Roberts & Haynes (1983) comment that mature seeds sink within 24 hours due to the absorption of water.
A. Ng, F.S.P. in Tree Flora of Malaya 2. 1973, B. Roberts, M.L. & R.R. Haynes in PI. Syst. Evol. 143. 1983, C. Thien, L.B., et al. in Amer. J. Bot. 70. 1983, D. White, D. A. & L.B. Thien, in J. Elisha Mitchell Sci. Soc. 101. 1985

Morphology

The floral structure in Illicium is primitive, with numerous spirally arranged organs around an elongated receptacle, and a regular perianth of unfused segments that do not form distinct sepals and petals . Although Illicium flowers tend to be comparatively uniform in structure, taxonomically significant variation is evident in several perianth characters, including tepal number, shape and colour. Keng (1965) has suggested that differences in tepal shape are correlated with the number of vascular bundles at the point of attachment to the receptacle: those with narrowly oblong, ligulate or lanceolate tepals possess a single main bundle at the base, whereas those with ovate to suborbicular tepals possess five or more basal bundles. Saunders (1995), however, has shown that all tepals in Illicium possess only a single basal vascular bundle, irrespective of their shape. The apparent distinction between the vascular patterns of the two tepal shapes is due to differences in the location of the dichotomous divisions of the vascular system: the bundle divides closer to the point of attachment in ovate to suborbicular tepals.
The number of stamens is also variable within the genus, and taxonomically valuable at the specific level. The filaments are short and thick, with a single broad vascular bundle, sometimes appearing as two separate bundles. The anthers have two lobes with two locules each, joined by a truncate connective, and show introrse or introrse-lateral dehiscence. The gynoecium consists of a whorl of free carpels that are attached laterally to the elongated receptacle; the number of carpels is also variable in the genus and taxonomically useful at the specific level.

Each carpel is differentiated into an enlarged ovary, short style and curved stigmatic crest with numerous papillae, and initially develops as a conduplicate structure (Robertson & Tucker 1979). Studies of mature floral structure, particularly with respect to the vasculature of filaments and carpels, indicate a putative reductive evolutionary trend in the genus (Keng 1965).
The floral ontogeny of several species has been described by Robertson & Tucker (1979), Erbar & Leins (1983), and Ronse Decraene & Smets (1993); the floral organs have been shown to develop in helical succession, with the carpels later appearing whorled.
E. Erbar, C. & P. Leins in Bot. Jahrb. Syst. 103. 1983, F. Keng, H. - in The families and genera of vascular plants. Vol. 2: Flowering plants. Dicotyledons. Berlin. 1993, G. Keng, H. in Bot. Bull. Acad. Sin. 6. 1965, H. Robertson, R.E. & S.C. Tucker in Amer. J. Bot. 66. 1979, I. Ronse Decraene, L.P. & E.F. Smets in Bot. J. Linn. Soc. 113. 1993, J. Saunders, R.M.K. in Bot. J. Linn. Soc. 117. 1995, K. Smith, A.C. in Sargentia 7. 1947

Taxonomy

The taxonomic position of Illicium has been the source of considerable discussion, although its affinities with the Magnoliales have long been recognised; this is reflected historically by its classification in both the families Magnoliaceae (e.g., Bentham & Hooker 1862) and Winteraceae (e.g., Ridley 1922). The treatment that is most widely accepted today (proposed by Smith 1947), involves the isolation of Illicium in the mono- typic family Illiciaceae on the basis of various morphological and anatomical criteria (discussed in detail by Bailey & Nast 1945, 1948). The Illiciaceae bear the closest relationship to the Schisandraceae, a small family of scrambling and twining woody vines. The isolated evolutionary position of these families has been recognised more recently by their classification as the sole members of the order Illiciales (e.g., Takhtajan 1980; Cronquist 1981); it is generally agreed, however, that the Illiciales were derived from a common ancestry with such orders as Magnoliales and Winterales, although the Illiciales are without very close modern relatives.

The last comprehensive revision of Illicium was the monograph by Smith (1947), who recognised 42 species. He divided the genus into two sections, viz. section Badiana Spach (which includes the type species and should therefore bear the autonym sect. Illicium), and section Cymbostemon (Spach) A.C. Sm. Section Illicium is characterised by narrowly oblong, ligulate or lanceolate inner perianth segments, and is represented in the Malesian flora by the distinctive species, /. philippinense Merr. The remaining six Malesian species belong to section Cymbostemon, which is characterised by generally ovate to suborbicular inner perianth segments. The two basic types of pollen in the genus (discussed above) are broadly correlated with the sectional distinctions, with tri- zonocolpate pollen occurring in sect. Illicium and trisyncolpate pollen in sect. Cymbostemon; although many of the Malesian species had not previously been studied palyno- logically, they are all shown by Saunders (1995) to conform to this taxonomic distinction.

The North American species I. floridanum (sect. Illicium) is atypical, however, since it possesses trisyncolpate grains (Wodehouse 1959; Lieux 1980).
P. Bailey, I.W. & C.G. Nast in J. Arnold Arbor. 26. 1945, Q. Bailey, I.W. & C.G. Nast in J. Arnold Arbor. 29. 1948, R. Bentham, G. & J.D. Hooker in Genera Plantarum 1. 1862, S. Cronquist, A. - in An integrated system of classification of flowering plants. 1981, T. Lieux, M.H. in Pollen et Spores 22. 1980, U. Ridley, H.N. in Flora of the Malay Peninsula 1. 1922, V. Saunders, R.M.K. in Bot. J. Linn. Soc. 117. 1995, W. Smith, A.C. in Sargentia 7. 1947, X. Takhtajan, A. in Bot. Rev. 46. 1980, Y. Wodehouse, R.P. - in Pollen grains. 1935, Z. Wodehouse, R.P. - in Pollen grains. 1959

Cytology

There is only one published chromosome count for a Malesian species of the genus Illicium: I. stapfii Merr. (syn. I. cauliflorum Merr.) is reported to have n = 14 and 2n = 28 (Ratter & Milne 1973). The same number has been reported for four extra-Malesian species (Morinaga et al. 1929; Whitaker 1933; Stone & Freeman 1968; Ehrendorfer et al. 1968; Okada 1975; Ratter & Milne 1976; Nagl et al. 1977), although the North American species I. floridanum has also been reported as n = 13 and 2n = 26 (Stone 1965; Stone & Freeman 1968). The base number for the genus is therefore regarded as x = 13, 14. As this base number is also shared by the closely related family Schisandraceae, Ehrendorfer et al. (1968) have suggested that these two families (collectively forming the order Illiciales) diverged from the basic Magnolialean stock and extinct precursors with x = 7 by dysploid reduction from the palaeotetraploid level of 2x = 14 to 2x = 13.
AA. Ehrendorfer, F., et al. in Taxon 17. 1968, AB. Morinaga, T., et al. in Bot. Mag. (Tokyo) 43. 1929, AC. Nagl, W., et al. in PI. Syst. Evol. 127. 1977, AD. Okada, H. in J. Sci. Hiroshima Univ. ser. B (Bot.), 15. 1975, AE. Ratter, J. A. & C. Milne in Notes Roy. Bot. Gard., Edinb. 32. 1973, AF. Ratter, J. A. & C. Milne in Notes Roy. Bot. Gard., Edinb. 35. 1976, AG. Stone, D.E. & J.L. Freeman in J. Arnold Arbor. 49. 1968, AH. Stone, D.E. in Madroño 18. 1965, AI. Whitaker, T.W. in J. Arnold Arbor. 14. 1933

Uses

The fruit of Illicium verum Hook. f. is the source of the spice Chinese Star Anise, used for flavouring food and liqueurs. Although this species does not occur in Malesia, the spice has been imported extensively from China and is traded in Malaysia as 'bunga lawang' or 'adas china' (Burkill 1966). The fruits of the Japanese species I. anisatum (syn. I. religiosum Siebold & Zucc.) are poisonous, although small quantities can be used for flavouring, and are sometimes retailed in Southeast Asia; confusion with the Chinese Star Anise resulted in unsuccessful attempts to grow it in Singapore (Burkill 1966). There has been considerable confusion regarding the application of common names to /. verum and I. anisatum (Small 1996). Although the name 'star anise' is rather ambiguous, it is widely used commercially; its use for the poisonous species I. anisatum should therefore be avoided. Other Illicium species have various reported medicinal properties, often as a stomachics, carminatives, stimulants or vermifuges (Perry 1980). The timber is of very limited value due to the small size of the trees.

None of the Malesian species is of any reported ethnobotanical value.
AJ. Burkill, I.H. in A dictionary of the economic products of the Malay Peninsula 2. 1966, AK. Perry, L.M. - in Medicinal plants of East and Southeast Asia. 1980, AL. Small, E. in Econ. Bot. 50. 1996

Phytochemo

Formerly Kadsura, Illicium and Schisandra were incorporated in Magnoliaceae. Later these three genera were united in a separate family called Schisandraceae s.l. (e.g. Gundersen 1950) or in two families, Illiciaceae (Illicium only) and Schisandraceae s.str. (.Kadsura and Schisandra). Hegnauer (1973, 1990) treated chemical characters of all three genera sub Schisandraceae s.l.; many references and structural formulae are available in these two reviews.

Summarizing, the following statements seem to be adequate today.

The three fore-mentioned genera are well known in oriental medicine, especially in China, Korea, Taiwan and Japan. They have yielded a considerable number of crude drugs. A lot of chemical work has been performed in recent times with several of these medicinal plants. Nevertheless our knowledge of their chemical characters is still rather fragmentary. As far as chemical constituents are known they allow some preliminary taxonomic conclusions.

The production of essential oils and their deposition in idioblastic oil cells is shared by all three genera. This is a character of woody polycarps. There are marked differences, however, in secondary metabolism of Kadsura and Schisandra on the one side and Illicium on the other. The following special features of natural product chemistry are known from several taxa of the first mentioned two genera. 1) Production and accumulation of biologically active lignans belonging mainly to three types. The most peculiar lignans of Kadsura and Schisandra are bibenzocyclo-octadienoid compounds, such as the gomisins, the schizandrins and many others; they seem to be biogenetically related with bibenzylbutanoid-type lignans, e.g. anwulignan, pregomisin and others. 2) Moreover, both genera produce characteristic lanostane-type tetracyclic triterpenic acids. Striking structural features of some of these triterpenoids are a seco-A-ring and/or a rearranged C/D- ring-junction. However, very recently, similar triterpenoids were isolated from fresh twigs and leaves of Illicium dunnianum (Sy et al. 1997).

Illicium contains several toxic species in Indochina, China, Korea, Taiwan, Japan, and the USA (I. floridanum ?; toxic constituents still unknown).

The toxins of I. anisatum L. (syn. L religiosum Siebold & Zucc.) were investigated thoroughly and shown to be rearranged, dilactonic, picrotoxin-like sesquiterpenoids. Anisatin, neoanisatin and the non-toxic pseudoanisatin became first known from fruits (pericarps and seeds) of /. anisatum (Japanese Star Anise or Shikimi). Anisatin and pseudoanisatin are convulsants. Fruits of /. anisatum later yielded two other, but bio- genetically related, types of C15-dilactones, I.c. the majucin-type 6-deoxymajucin (Kouono et al. 1988) and the anislactone-type anislactones A and B (Kouono et al. 1990). Recently (Okuyama et al. 1993) trace amounts of anisatin-derivatives, I.c. veranisatin A and B, have been isolated from the spice Chinese Star Anise, which is derived from a cultigen of southern China and northern Vietnam that is known as /. verum Hook. f. The negligible amounts of these two new convulsants present in the fruits of I. verum are however without risk for their medicinal and culinary uses by man. Still another type of C15-dilactones was detected in wood of /. tashiroi\ two compounds were isolated and called illicinolide A and B (Fukuyama et al. 1992a). The same wood also yielded tashironin, C22H26O6, which was shown to be the monobenzoate of a tricyclic rearranged sesquiterpenetriol; tashironin may be related to the C15-progenitor of the Illicium-dilactones (Fukuyama et al. 1995). Toxic C15-dilactones are presently known also from I. dunnianum Tutcher (Yang et al. 1988) and I. majus Hook. f. & Thomson.

The essential oils of fruits, leaves, barks, woods and other parts of Illicium taxa contain mainly phenylpropanoids, e.g. chavicol, eugenol, safrol and related propenyl- and allylbenzenoids, and mono- and sesquiterpenes. Their composition depends on taxa and plant parts. Anethol (= O-methylanol = p-methoxypropenyl-benzene) is the predominant oil constituent of Chinese Star Anise. Bark of I. difengpi B.N. Chang, a non-toxic Chinese taxon, also produces the rutinoside of 2-hydroxy-safrol and several derivatives of a dihydroconiferylalcohol 4-glycerinether (Kouono et al. 1992).

A tendency to prenylate phenylpropanoids in various ways is a special feature of Illicium taxa. O-Prenylation yields natural products like O-prenyleugenol and illicinol (= 2- prenyloxysafrol). C-Prenylation combined with reductions, rearrangements and cycliza- tions generates the so-called phytoquinoids, the illicinones and illifunones (Yakushijin et al. 1980,1984). Wood of I. tashiroi Maxim, yielded many illicinones and illifunones. Illicinone E is one of its main constituents; it is accompanied by a whole array of derivatives, some of which are chlorinated (Fukuyama et al. 1992b, 1994).

In a number of Illicium taxa illicinones and illifunones seem to be replaced by lignane- like C6-C3-dimers and -trimers. Biphenyl-type neolignans (magnolol, honokiol) and tri- phenyl-type sesquineolignans (dunnianol, macranthol, simonsinol) were isolated from Chinese material of I. dunnianum, I. macranthum A.C. Sm., I. majus and L simonsii Maxim. (Kouono et al. 1994). Otherwise, I. difengpi and I. majus seem to produce predominantly neolignans of the aryldihydrobenzofuranpropanol-type. One of the neolignans of the bark of I. difengpi was shown to be identical with sakuraresinol, a glycerin ether already known from the bark of Prunus jamasakura Koidz. (Kouono et al. 1993).

Shikimic acid is one of the precursors of aromatic plant constituents. It was first isolated from fruits of I. anisatum (Shikimi) where it is present in large amounts and is accompanied by protocatechuic acid. Common plant phenolics such as hydroxybenzoic and hydroxycinnamic acids, flavonoids and proanthocyanidins seem to be ubiquitous in Illicium; however, their chemical investigation was rather neglected hitherto. Glycosides of the flavonols kaempferol and quercetin (isoquercitrin isolated from Illicium material) were detected in every investigated species including the American I. floridanum Ellis. The only recent investigations of common phenolics concern herbarium leaves of I. manipurense Watt ex King (Williams & Harvey 1982) and fresh bark of I. anisatum (Mori- moto et al. 1988). The latter contains catechin, 6- and 8-prenylcatechin and much pro- cyanidins of which several dimeric and trimeric compounds were isolated.

The foregoing summary is based predominantly on investigations of Chinese, Taiwanese and Japanese (including the Ryukyus) plant material. Southern China, Taiwan and the Ryukyu Islands seem to be together the present centre of diversification of Illicium and the precise systematic status of many described taxa is still questionable. The following taxa are mentioned in recent phytochemical literature: I. arborescens, I. difengpi, I. dunnianum, I. macranthum, I. majus, I. manipurense, I. religiosum, I. simonsii, I. tashiroi, and I. verum.

The toxic dilactonic sesquiterpenes (anisatin, majucin, anislactones etc.), modified isoprenylated phenylpropanoids (illicinones, illifunones), prenylated catechins and bi- phenyl-type neolignans represent outstanding chemical features of Illicium. Such compounds have not yet been detected in Kadsura and Schisandra. Secondary metabolism, therefore, seems to agree with the treatment of Illicium as a separate family.

Johnson (1954) and Johnson & Fairbrothers (1965) have used serological techniques to verify the assertion by Smith (1947) that the genus does not have a close relationship with the Magnoliales.
AM. Fukuyama, Y., et al. in Phytochemistry 31, AN. Fukuyama, Y., et al. in Phytochemistry 36. 1994, AO. Fukuyama, Y., et al. in Phytochemistry 37. 1994, AP. Fukuyama, Y., et al. in Tetrahedron 48, AQ. Fukuyama, Y., et al. in Tetrahedron Letters 36. 1995, AR. Gundersen, A. - Families of dicotyledons in Chronica Botanica, Waltham, Mass. 1950, AS. Hegnauer, R. in Chemotaxonomie der Pflanzen 6. 1973, AT. Hegnauer, R. in Chemotaxonomie der Pflanzen 9. 1990, AU. Johnson, M. A. & D.E. Fairbrothers in Bot. Gaz. 126. 1965, AV. Johnson, M. A. in Serol. Mus. Bull. 13. 1954, AW. Kouono, I., et al. in Chem. Pharm. Bull. 36. 1988, AX. Kouono, I., et al. in Chem. Pharm. Bull. 38. 1990, AY. Kouono, I., et al. in Chem. Pharm. Bull. 40. 1992, AZ. Kouono, I., et al. in Chem. Pharm. Bull. 42. 1994, BA. Kouono, I., et al. in Phytochemistry 32. 1993, BB. Morimoto, S., et al. in Phytochemistry 27. 1988, BC. Okuyama, E., et al. in Chem. Pharm. Bull. 41. 1993, BD. Smith, A.C. in Sargentia 7. 1947, BE. Sy, L.-K., et al. in Phytochemistry 44. 1997, BF. Williams, C. & W.J. Harvey in Phytochemistry 21. 1982, BG. Yakushijin, K., et al. in Chem. Pharm. Bull. 28. 1980, BH. Yakushijin, K., et al. in Chem. Pharm. Bull. 32. 1984, BI. Yang, C.-S., et al. in Tetrahedron Letters 29. 19881. R. Hegnauer

Embryology

Microsporogenesis (Hayashi 1960) and megasporogenesis and embryology (Hayashi 1963) have been described in detail for Illicium anisatum. The development of the embryo sac appears to conform to the Polygonum type, and the development of the embryo is of the Asterad type.
BJ. Hayashi, Y. in Sci. Rep. Tohoku Univ., ser. IV (Biol.), 26. 1960, BK. Hayashi, Y. in Sci. Rep. Tohoku Univ., ser. IV (Biol.), 29. 1963

Citation

Ng - in Tree Fl. Malaya. 1973: 253
R.M.K. Saunders - in Tree Fl. Sabah & Sarawak. 1995: 227
R.M.K. Saunders - in Bot. J. Linn. Soc. 1995
A.C. Sm. - in Sargentia. 1947: 10
L. - in Gen. PL. 1764: 244
Ridl. - in Fl. Malay Penins. 1922: 18