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2Department of Biology, Colorado State University, Fort Collins, Colorado 80523; and 4Department of Botany, NHB-166, Smithsonian Institution, Washington, D.C. 20560
Received for publication October 30, 1998. Accepted for publication March 9, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Aralia • Araliaceae • ginseng • Panax • pollen ultrastructure
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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65 genera of flowering plants that demonstrate a classical eastern Asian and eastern North American disjunct distributional pattern (Gray, 1859
; Li, 1952
; Graham, 1972
; Wen, 1998
). It consists of 12 species, ten from eastern Asia and two from eastern North America (Wen and Zimmer, 1996
). Despite the long history of scientific interest in this biogeographical pattern, few studies have documented the differentiation of pollen morphology and ultrastructure between the eastern Asian and eastern North American disjuncts.
Panax, commonly known as the ginseng genus, is medicinally important in the Orient, where almost every species of the genus has been used as a source of medicine. Three of the species [P. ginseng C. A. Meyer (ginseng), P. quinquefolius L. (American ginseng), and P. notoginseng (Burkill) F. H. Chen (sanchi)] are highly regarded medicines in China and therefore widely cultivated. Ginseng literally means the essence of man (Hu, 1976
) and is known as the lord or king of herbs. Chinese have used it for over 2000 years as a tonic, a stimulant, and a fatigue-resisting medicine, although it is considered a medical enigma by some scientists (e.g., Lewis, 1986
; Duke, 1989
).
An evolutionary hypothesis of Panax, based on triterpenoids, was proposed by Zhou et al. (1975)
. Panax was divided into two major groups, with the three medicinally most important species, P. ginseng, P. notoginseng, and P. quinquefolius, forming a primitive group (Group I), and the remaining species forming a more advanced group (Group II). No evolutionary relationships within each group were hypothesized. A recent molecular phylogenetic study of Panax based on sequences of the internal transcribed spacer (ITS) regions of nuclear ribosomal DNA (Wen and Zimmer, 1996
) suggested that (1) P. trifolius L. from eastern North America is phylogenetically basal within Panax; (2) P. notoginseng does not form a monophyletic group with P. ginseng and P. quinquefolius, as suggested by Zhou et al. (1975)
; (3) the eastern North American P. quinquefolius (American ginseng) is closely related to the eastern Asian P. ginseng (ginseng), but no sister-group relationship was suggested between the two taxa; and (4) species of Panax (P. trifolius excepted) are closely related to each other.
Panax is considered closely related to Aralia L., a genus of 51 species in Asia and the Americas (Harms, 1897
; Wen, 1993
; Wen and Zimmer, 1996
). Using Aralia as the outgroup, the monophyly of Panax is supported by the following morphological synapomorphies: palmately compound leaves, whorled leaf arrangement, a single terminal inflorescence, and a bi- or tricarpellate ovary.
In an effort to provide a comprehensive taxonomic and phylogenetic study of Panax and its relatives, we examined the pollen ultrastructure of Panax. Most previous studies of pollen of Araliaceae have been based on observations using light microscopy (LM) and scanning electron microscopy (SEM). To date, there has been only one report of pollen morphology of Araliaceae based on transmission electron microscopy (TEM), in which Tseng et al. (1983)
sectioned two species of Acanthopanax (Decne. & Planchon) Miq. (= Eleutherococcus Maxim.).
Erdtman (1966)
, using LM, examined the pollen of 30 species representing 20 genera of Araliaceae. He described it as mostly 3-colporate with lalongate ora, usually reticulate, and noted that the sexine was often thicker at the poles than at the equator.
More detailed descriptions of Araliaceae pollen have been provided by Tseng and his collaborators in a series of papers (Tseng, 1971, 1973, 1974
; Shoup and Tseng, 1977
; Tseng and Shoup, 1978
; Tseng et al., 1983
) and by Shang and Callen (1988)
, based mostly on LM and SEM. Tseng (1971)
characterized the pollen wall of some Tetraplasandra A. Gray as being thicker at the poles from elongate bacula (= columellae) and as having a nexine-2 (= endexine) reaching a maximum dimension at the margins of the os (= endoaperture). Although he did not specifically refer to the accumulation of endexine along each side of the colpus, some of his 1-µm sections do show this condition, e.g., figs. 3o, 4g, 6g, 7n, and 8f. Tseng (1973)
reported that all species examined of Tupidanthus Hook.f. & Thomson and Plerandra A. Gray have a thickened nexine along the aperture border.
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assessed the pollen variation by multivariate analysis. Using this methodology, he identified two pollen types within Polyscias: one consisting of small grains with microreticulate tecta and lalongate ora and a second with large grains, either reticulate tecta or intectate, and lalongate, circular, or lolongate ora. For the most part, the two types were congruent with sectional boundaries. But all species examined have a localized thickening of the exine bordering the ora. The objectives of this study were to: (1) examine and compare pollen ultrastructure of Panax; and (2) test the phylogenetic congruence of pollen and ribosomal DNA data. We describe and illustrate the morphology and exine structure of ten species of Panax and six species of Aralia. All pollen samples were examined in TEM as well as LM and SEM.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. For LM, pollen was mounted in glycerin jelly and sealed with paraffin.
For SEM, pollen was pipetted in 60% ethyl alcohol on a specimen stub, allowed to dry, and sputter-coated with carbon and then gold palladium. Pollen was examined and photographed with a Hitachi 570 scanning electron microscope.
For TEM, the acetolyzed pollen was first concentrated in 1.5% agar, stained with osmium tetroxide, then uranyl acetate, and embedded in L. R. White plastic resin. After sectioning with a diamond knife, the sections were stained with lead citrate and then examined and photographed with a JEOL 1200EX TEM.
The species examined, voucher data, illustration figures, and pollen size are given in Table 1. Measurements of polar and equatorial axes were made from ten acetolyzed grains in LM.
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, but define three terms here for the convenience of the reader: infratectum = a general term for the layer beneath the tectum, which may be granular, columellar, or structureless; costa ectocolpi = thickenings of the endexine bordering (to each side of) the colpus; and costa endocolpi = thickenings of the endexine bordering a lalongate endoaperture. The pollen descriptions are based on all the micrographs, not just those in Figs. 1–68 and are organized as follows: morphological characteristics and measurements are based on LM and SEM; and structural characteristics are based on TEM. The measurements given in the pollen descriptions represent the range of the genus or species based on the collections examined here.
Although the pollen description of Aralia is based on only six of the 51 species, each of the six was examined in LM, SEM, and TEM. Given the paucity of exine structure information for Araliaceae, we provide a pollen description of Aralia, which should, however, be treated with caution.
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RESULTS |
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Panax L., Figs. 1–36, 41–43, 65, 66, and 68
P. bipinnatifidus Seemann, P. ginseng, P. japonicus C. A. Meyer, P. major Ting, P. notoginseng, P. pseudoginseng Wallich, P. quinquefolius, P. sinensis J. Wen, and P. wangianus Sun.
Pollen prolate spheroidal, subprolate (Fig. 68), or prolate in equatorial (E) view (Figs. 1, 33); in one species (P. ginseng, Figs. 6, 9, 65) the poles slightly flattened; triangular or rounded triangular in polar (P) view (Figs. 10, 26, 41); 22.7–40.3 µm P x 20.8–33.8 µm E; 3-colporate, rarely 4-colporate (some grains of P. japonicus) or in one collection (P. ginseng, cultivated) some grains 3-colporoidate, the colpal margins inwardly curved (Figs. 3, 22, 33), costa ectocolpi present (in LM, a dark streak to each side of colpus; Figs. 66, 68), occasionally a colpal ridge (Fig. 27); the endoaperture mostly lalongate with diffuse lateral margins (Figs. 66, 68), the polar margins (above and below) thickened (some grains of P. ginseng excepted) and forming costa endocolpi (Figs. 2 [inset], 35, 42, 66, 68); the tectum mostly complete, conspicuously striato-reticulate (Figs. 15, 17, 36) to weakly striato-reticulate (the individual lira poorly defined) (Figs. 3, 9, 22, 41), or rarely with irregularly shaped perforations (many grains of P. ginseng; Fig. 6). In thin section, the nonapertural endexine thin (e.g., Figs. 2, 7, 32 [inset]); the apertural endexine thickened, frequently filling the shallow arch of the incurved margins of the colpus (e.g., Figs. 2, 18, 26, 31, 34) and forming costa ectocolpi, sometimes with a gap or marked thinning at the boundary of the apertural and nonapertural endexine (arrows in Figs. 10, 12, 32, 34); the foot layer thick (Figs. 5, 7, 14, 28, 32 [inset]), or seemingly thin (Figs. 4, 21, 25; but this appearance may be an artifact of staining); the columellae mostly short and slender (Figs. 4, 5, 7, 14, 32), occasionally longer and/or irregular in shape (Figs. 2, 23, 23 [inset], 35), in many species the columellae longer at the poles (Figs. 23, 35), in one species (P. ginseng, Figs. 4, 5, 7) with granules interspersed among the columellae; the tectum continuous (Figs. 7, 14, 42) or nearly so (Figs. 20, 25).
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and Ferguson (1977)
referred to this type of endoaperture as H-shaped, in which the sides of the "H" are the areas of marked thinning of the endexine. But our designation of V-shaped is based on a thickening of endexine. The fundamental tectum in pollen of Panax is striato-reticulate with the extremes represented by some grains of P. ginseng (Fig. 6) in which the lirae are not identifiable and by P. japonicus (Figs. 15, 17) in which the lirae are the most well-defined and separated from each other. Bridging this gap are the tecta of P. quinquefolius (Fig. 30), P. wangianus (Fig. 43), P. major (Fig. 24), P. bipinnatifidus (Fig. 3), P. notoginseng (Fig. 29), and P. sinensis (Fig. 36), listed in order of increasingly distinct lirae.
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Pollen of Panax ginseng of the collection of Wen 1250 is distinguished by a thick, almost continuous tectum (Fig. 4) in which much of the distinction of the lirae has been lost (Fig. 6), slightly flattened poles, and an infratectum of short columellae and sparse small granules (Fig. 4). The poor separation of the foot layer and nonapertural endexine (Fig. 4) is probably an artifact of staining. Considering the wide interest in the medicinal properties of P. ginseng and thus in any closely related taxa, we attempted to confirm the type of pollen found in the collection of Wen 1250 with pollen from another population. After much effort, a sample was obtained from a herbarium specimen (LH) of cultivated plants from the Imperial Gardens (Table 1) in Seoul, Korea. The exine structure of this cultivated collection (Figs. 5, 7) is similar to that of Wen 1250 (Fig. 4) with thick tecta, fine granules interspersed among the short columellae, and thick foot layers, but has a wider range of tectal variation. Although many grains of the cultivated collection (Fig. 9) have tecta similar to those of the collection of Wen 1250 (Fig. 6), there are other grains that have striato-reticulate tecta (Fig. 8) in which short lirae are identifiable. Other variations of the cultivated collection include individual grains with more than one tectal morphology—irregularly gemmate areas and psilate areas, the latter possibly demonstrating the ultimate loss of lira distinction. The difference in the tectum of the tangential section in Fig. 5 could be explained by the grain having a more striato-reticulate morphology from 11 o'clock to six and gemmate morphology from six to 11. Panax ginseng is a clearly marked species, and there is no possibility of misidentification.
Pollen of the two collections of Panax japonicus also shows tectal variation. In SEM, all grains from Bisset 3720 (Fig. 17) and some from Nakaike s.n. (Fig. 15) have the most well-defined lirae of all Panax collections examined (P. trifolius excepted), i.e., long, branched and only loosely interwoven, almost as if the lirae were deposited individually. In TEM, the outer surface (Figs. 14, 16) shows extensions and fragments of lirae, reinforcing the SEM observations. However, the collection of Nakaike s.n. has some grains in which the lirae are not so distinct (Fig. 13, upper and lower grains). Pollen from two collections of P. quinquefolius (Table 1) is more uniform.
Panax trifolius, Figs. 37–40, 67
Pollen prolate (Figs. 40, 67) in equatorial view; 40.3–50.7 µm P x 27.3–36.4 µm E; 3-colporate, costa ectocolpi present but not conspicuous; the endoaperture lalongate with diffuse lateral margins (Fig. 67), the polar margins thickened and forming costa endocolpi; the tectum complete or nearly so (Fig. 40), prominently striate (Figs. 39, 40). In thin sections, the nonapertural endexine thin; the apertural endexine thick, forming costa endocolpi (Fig. 38); gaps or thinning of the endexine at the boundary between apertural and nonapertural not observed in the collections examined; the foot layer thick (Fig. 37); the columellae large, even massive (Fig. 37), occasionally branched or seemingly fused; the tectum mostly continuous (Fig. 28), the inner surface finely and irregularly granular (Fig. 37).
Pollen of Panax trifolius has very large columellae (Figs. 37, 38) in sharp contrast to the small columellae found in the remaining nine examined species of Panax (Figs. 2, 4, 7, 12, 14, 21, 25, 32, 35, 42). The tectum has a granular inner surface and is prominently striate (Figs. 39, 40) vs. psilate inner surfaces and striato-reticulate (Figs. 15, 17, 36) or weakly striate reticulate (Figs. 19, 43), and the lirae are larger in diameter. Such striate tecta and very large columellae are unknown in the pollen of any other members of Araliaceae examined. Grains of P. trifolius are the largest of the ten species examined (Table 1).
Aralia L., Figs. 44–64
A. californica S. Wats., A. hispida Vent., A. humilis Cav., A. leschenaultii (DC.) J. Wen, A. nudicaulis L., and A. spinosa L. Pollen mostly subprolate in equatorial view (Figs. 50, 51), triangular (Fig. 44) to rounded triangular (Figs. 55, 61) in polar view; 3-colporate, the colpal margins incurved (Figs. 47, 50, 51, 59), sometimes with a colpal ridge (Figs. 51, 62), costa ectocolpi variable, from poorly developed (A. californica, A. humilis) to more prominent (A. leschenaultii [Fig. 48], A. nudicaulis); the endoaperture mostly lalongate, frequently with diffuse lateral margins (A. hispida excepted), costa endocolpi variable, small but sharply delimited (A. californica) to more prominent (A. leschenaultii); the tectum variable, complete, and punctate (Fig. 51), incomplete, and finely reticulate (Fig. 64) with perforations larger at the poles (A. spinosa), incomplete and perforate (Figs. 44, 57) to irregularly perforate (Figs. 47, 59), or weakly striato-reticulate (A. leschenaultii, Figs. 49, 50). In thin sections, the nonapertural endexine thin (Figs. 48, 60); the apertural endexine thickened at the colpi, sometimes (partially) filling the arch of the ectexine (A. californica; A. hispida, Fig. 54; A. leschenaultii, Fig. 48, arrowheads), sometimes with a gap or marked thinning at the boundary of nonapertural and apertural endexines (A. californica; A. hispida [Fig. 54, arrow]; A. leschenaultii [Fig. 48, arrow]); the foot layer thin (Figs. 45, 52, 53) to thick (Fig. 63); the columellae very short (Figs. 45, 48, 60), sometimes elongated at the poles (conspicuously so in A. spinosa); the tectum variable, continuous, or nearly so (Fig. 54) to more discontinuous (Figs. 60, 63).
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Pollen of Aralia spinosa (Figs. 62–64) is thicker walled and has elongated columellae at the poles, characteristics easily seen in LM. The colpal ridge (Figs. 62, 63) is formed by a thicker foot layer, slightly longer columellae, and a modest accumulation of endexine. Although not conspicuous in the whole grain shown in Fig. 62, many others have larger tectal perforations at the poles.
In pollen of A. nudicaulis (Figs. 58–61), although the surface depressions in Fig. 59 could be interpreted as shallow indentations of the tectum, they are actually the upper surface of the foot layer (arrows in Figs. 59, 60) in a very thin-walled exine.
Of the six species, only pollen of Aralia leschenaultii (Figs. 48–50), formerly assigned to Pentapanax Seem., has a weakly striato-reticulate tectum. However, in a continuing study of pollen of Aralia, eight of ten species examined had striato-reticulate tecta similar to those illustrated in Figs. 19, 24, 30, and 43.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), white petals, 3-locular ovary, and dry fruits. Its phylogenetic position was hypothesized as basal within Panax based on the ITS sequences of the nuclear ribosomal DNA (Wen and Zimmer, 1996
). The pollen data support this hypothesis. Because of the lack of very large columellae and highly striate tectum in Aralia, the close relative of Panax, we consider the distinct exine structure of P. trifolius as specialized.
The pollen data do not support the species group, P. ginseng, P. notoginseng, and P. quinquefolius, that Zhou et al. (1975)
recognized based on triterpenoids nor the species-pair relationship between P. ginseng and P. quinquefolius suggested by Li (1942, 1952, 1972)
. Subtle differences separate the pollen of the three species. Both collections of P. ginseng have pollen with thick, almost continuous tecta and an infratectum of short columellae and sparse granules. Pollen of P. notoginseng has a thinner, discontinuous, striato-reticulate tectum with well-defined lirae. Pollen of P. quinquefolius has a thinner, discontinuous, and weakly striato-reticulate tectum. Neither P. notoginseng nor P. quinquefolius has pollen with an infratectum like that of P. ginseng. Furthermore, in the recently reconstructed ITS phylogeny of Panax, Wen and Zimmer (1996)
did not detect a sister-group relationship between eastern Asian P. ginseng and eastern North American P. quinquefolius, suggesting the antiquity of the intercontinental disjuncts.
Panax japonicus has a distinctive tectum in comparison with other species of Panax.
This report is one of the few palynological observations made for the eastern Asian and eastern North American disjunct taxa. Nowicke and Skvarla (1981)
documented the distinctions of pollen morphology of several disjunct genera in Berberidaceae (e.g., Caulophyllum Michaux, Diphylleia Michaux, and Jeffersonia Barton), in which subtle differences in the pollen were observed among the Asian and North American disjuncts.
Pollen grains of Aralia and Panax have similar complex apertures, frequently short columellae, and overlapping tectal sculptures, suggesting a close relationship. Panax was treated as part of Aralia by several early workers (e.g., Decaisne and Planchon, 1854
; Bentham and Hooker, 1867
; Hooker, 1879
). Hutchinson (1967)
, however, placed Panax and Aralia in different tribes: Panaceae and Aralieae, respectively. This treatment has been criticized for being arbitrary by later workers (e.g., Hoo and Tseng, 1978
). The close relationship between Panax and Aralia is also supported by the relatively low sequence divergence of nuclear ribosomal DNA of species of Panax from those of Aralia (Wen and Zimmer, 1996
).
Pollen of Aralia spinosa from eastern North America is distinctive within the six species examined because of its thick wall. The columellae are conspicuously elongated at the poles where the exine can be up to 3 µm thick. Most grains have larger lumina at the poles, a characteristic that Henwood (1991)
found in Polyscias. But this characteristic occurs elsewhere and in unrelated families, e.g., Euphorbiaceae (Nowicke, Takahashi, and Webster, 1998
). Aralia spinosa and 24 species from eastern and southeastern Asia constitute Aralia sect. Dimorphanthus, which were characterized, in part, by pollen with the largest tectal perforations in the genus (Wen, 1991
). Whether all 24 species have the same exine structure as A. spinosa remains unanswered.
Aralia nudicaulis is a morphologically very distinct species within Aralia and is the sole member of Aralia sect. Nanae (Harms, 1897
; Wen, 1991
; Tseng et al., 1993
). It is a small unarmed clonal herb under the forest canopy of eastern North America. It has long horizontal rhizomes and lacks aerial stems. There is only one leaf and one small inflorescence consisting of three umbels arising from the ground. Its very thin exine may represent an extreme reduction.
Pollen of the nine species examined of Panax and of the six species of Aralia share similar apertures: an accumulation of endexine under the arch of ectexine along the colpus forming costa ectocolpi, and a thinning or break in the endexine at the boundary between apertural and nonapertural areas. This aperture structure occurs in other families, e.g., Cornaceae (Ferguson, 1977
) and Loasaceae (Poston and Nowicke, 1993
). At least some species of Panax and Aralia have pollen with the H-shaped endoapertural thinnings described and illustrated by Ferguson (1977)
and by Tseng (1971)
. Recent molecular phylogenetic studies suggested that Araliaceae, Cornaceae, and Loasaceae are closely related (Olmstead et al., 1993
; Xiang and Soltis, 1998
). This H-shaped aperture structure thus may be a palynological synapomorphy for Araliaceae, Cornaceae, Loasaceae, and their close allies.
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FOOTNOTES |
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3
Author for correspondence (jwen{at}lamar.ColoState.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Decaisne, J., and J. E. Planchon. 1854 Esquisse d'une monographie des Araliacees. Revue Horticole 1854: 104–109 (in French).
Duke, J. A. 1989 Ginseng: a concise handbook. Reference Publications, Inc., Algonac, MI.
Erdtman, G. 1966 Pollen morphology and plant taxonomy: angiosperms. Almquist and Wiksell, Stockholm.
Ferguson, I. K. 1977 Cornaceae Dum. World Pollen and Spore Flora 6: 1–34.
Graham, A. [ed.]. 1972 Floristics and paleofloristics of Asia and eastern North America. Elsevier, Amsterdam.
Gray, A. 1859 Diagnostic characters of new species of phanerogamous plants collected in Japan by Charles Wright, botanist of the U.S. North Pacific Exploring Expedition. (Published by request of Captain James Rodgers, Commander of the Expedition.) With observations upon the relations of the Japanese flora to that of North America, and to other parts of the northern temperate zone. Memoirs of the American Academy of Arts 6: 377–452.
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Hoo, G., and C.-J. Tseng. 1978 Angiospermae, Dicotyledoneae, Araliaceae—Flora Reipublicae Popularis Sinicae, vol. 54. Science Press, Beijing (in Chinese).
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———. 1952 Floristic relationships between eastern Asia and eastern North America. Transanctions of American Philosophical Society 42: 371–429.
———. 1972 Eastern Asia–eastern North America species-pairs in wide-ranging genera. In A. Graham [ed.], Floristics and paleofloristics of Asia and eastern North America, 65–78. Elsevier, Amsterdam.
Nowicke, J. W., and J. J. Skvarla. 1981 Pollen morphology and phylogenetic relationships of the Berberidaceae. Smithsonian Contributions to Botany 50.
———, M. Takahashi, and G. L. Webster. 1998 Pollen morphology, exine structure and systematics of Acalyphoideae (Euphorbiaceae). Part 1. Tribes Clutieae (Clutia), Pogonophoreae (Pogonophora), Chaetocarpeae (Chaetocarpus, Trigonopleura), Pereae (Pera) Cheiloseae (Cheilosa, Neoscortechinia), Dicoelieae (Dicoelia), Galearieae (Galearia, Microdesmis, Panda) and Ampereae (Amperea, Monotaxis). Review of Palaeobotany and Palynology 102: 115–152.[ISI]
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Poston, M. E., and J. W. Nowicke. 1993 Pollen morphology, trichome types, and relationships of the Gronovioideae (Loasaceae). American Journal of Botany 80: 689–704.[CrossRef][ISI]
Punt, W., S. Blackmore, S. Nilsson, and A. Le Thomas. 1994 Glossary of pollen and spore terminology. LPP Contributions Series Number 1, Utrecht.
Schlessman, M. A. 1987 Gender modification in North American ginsengs. BioScience 37: 469–475.
———. 1990 Phenotypic gender in sex changing dwarf ginseng, Panax trifolium (Araliaceae). American Journal of Botany 77: 1125–1131.[CrossRef][ISI]
———. 1991 Size, gender, and sex change in dwarf ginseng, Panax trifolium (Araliaceae). Oecologia 87: 588–595.[CrossRef][ISI]
Shang, C.-B., and D. Callen. 1988 Pollen morphology of the family Araliaceae in China. Bulletin of Botanical Research (China) 8: 13–35, plates 1–13 (in Chinese with English summary).
Shoup, J. R., and C. C. Tseng. 1977 A palynological study of Schefflera paraensis Huber ex Duke (Araliaceae). Grana 16: 81–84.
Tseng, C. C. 1971 Light and scanning electron microscopic studies on pollen of Tetraplasandra (Araliaceae) and relatives. American Journal of Botany 58: 505–516.[CrossRef][ISI]
———. 1973 Systematic palynology of Tupidanthus and Plerandra (Araliaceae). Grana 13: 51–56.
———. 1974 Pollen of Boerlagiodendron: a unique type in the Araliaceae. American Journal of Botany 61: 717–721.[CrossRef][ISI]
———, and J. R. Shoup. 1978 Pollen morphology of Schefflera (Araliaceae). American Journal of Botany 65: 384–394.[CrossRef][ISI]
———, ———, T.-I. Chuang, and W. C. Hsieh. 1983 Pollen morphology of Acanthopanax (Araliaceae). Grana 22: 11–17.
———, J. Wen, K. L. Hedges, and Y. C. Chen. 1993 Computer-based protein profile analysis in Aralia (Araliaceae). Cathaya 5: 69–79.
Wen, J. 1991 Systematics of Aralia (Araliaceae). Ph.D. dissertation, Ohio State University, Columbus, OH.
———. 1993 Generic delimitation of Aralia (Araliaceae). Brittonia 45: 47–55.[CrossRef][ISI]
———. 1998 Evolution of the eastern Asian and eastern North American disjunct pattern: insights from phylogenetic studies. Korean Journal of Plant Taxonomy 28: 63–81.
———, and E. A. Zimmer. 1996 Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 6: 167–177.[CrossRef][ISI][Medline]
Xiang, Q.-Y., and D. E. Soltis. 1998 RbcL sequence data define a cornaceous clade and clarify relationships of Cornaceae sensu lato. University Museum, University of Tokyo, Bulletin 37: 123–137.
Zhou, J., W.-G. Huang, M.-Z. Wu, C.-R. Yang, K.-M. Feng, and Z.-Y. Wu. 1975 Triterpenoids from Panax Linn. and their relationship with taxonomy and geographical distribution. Acta Phytotaxonomica Sinica 13(2): 29–45, plates 6–7 (in Chinese with English summary).
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