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Systematics |
Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing 100093, P. R. China
Received for publication September 27, 2001. Accepted for publication December 20, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: androecium • Chloranthaceae • Chloranthus • ITS sequences • phylogeny • trnL-F sequences
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Endress, 1987
; Todzia, 1993
; Eklund, 1999
). Extant species of Chloranthus mainly occur in eastern and southern Asia (Wu, 1982
; Verdcourt, 1992
; Kong, 2000a
), while evidence from paleobotany indicates that Chloranthus-like plants were well established in Europe and North America during the Late Cretaceous and probably disappeared from these areas during the Tertiary or Quaternary as a result of changed climate conditions (Friis, Crane, and Pedersen, 1986
; Crane, Friis, and Pedersen, 1989
; Herendeen, Crepet, and Nixon, 1993
; Eklund, Friis, and Pedersen, 1997
; Eklund, 1999
).
Current estimates of the size of the genus vary depending upon the monographer and the choice of characters used to delimit taxa. Wu (1982)
, for instance, recognized 17 species (of which 13 are recorded in China) and Verdcourt (1992)
20, whereas Todzia (1993)
and Liu (1996)
accepted 18 and 10 species, respectively. The disagreement between treatments is mainly due to the insufficient knowledge of variation patterns of many morphological characters. Chloranthus anhuiensis K. F. Wu and C. monostachys R. Br., for example, were shown to be plants of C. serratus (Thunb.) Roem. et Schult. at later stages of development, and C. multistachys P'ei and C. hupehensis Pamp. were later developmental stages of C. henryi Hemsl. (Wang, Huang, and Wu, 1984
; Kong, 2000a
). Besides, C. elatior Link and C. holostegius (Hand.-Mazz.) P'ei et Shan were found indistinguishable from C. erectus (Buch.-Ham.) Verdc. and C. nervosus Coll. et Hemsl., respectively (Verdcourt, 1986
, 1992
). In our recent monograph of the genus Chloranthus, ten species are recognized, and the problem that now faces us is how to arrange them systematically to reflect our current knowledge of relationships among them.
Growth habit and androecium morphology have been used as primary characters to delimit species of Chloranthus. Based mainly on habit, Solms-Laubach (1869)
divided Chloranthus sensu lato (s.l.) (including also Sarcandra Gardn.) into two groups, i.e., subgenera Fruticosi and Herbacei. The former subgenus contains four suffrutescent species, and the latter, four herbaceous species. Solms-Laubach also divided subgen. Fruticosi into sections Triandri and Monandri, and subgen. Herbacei into sections Brachyuri and Macronuri, on the basis of androecium morphology. Bentham and Hooker (1880)
, however, stressed the characteristics of androecial organs and recognized three sections in Chloranthus s.l.: Euchloranthus, Tricercandra, and Sarcandra. Species of Euchloranthus (= Triandri + Brachyuri) are characterized by their tripartite androecium with short connectives, while those of Tricercandra (= Macronuri) by their tripartite androecium with distinctly long connectives. Section Sarcandra (= Monandri) is characterized by an undivided androecium. Nakai (1930)
gave Bentham and Hooker's sections generic ranks, and thus split Chloranthus s.l. into three genera: Chloranthus sensu stricto (s.s.), Tricercandra A. Gray, and Sarcandra Gardn. Up to date, the separation of Sarcandra from Chloranthus has been widely accepted, while species of Tricercandra were still included in Chloranthus (e.g., Swamy and Bailey, 1950
; Swamy, 1953
; Wu, 1982
; Endress, 1986
, 1987
; Todzia, 1993
; Eklund, 1999
). Within Chloranthus, the majority of researchers reticently divided the genus into two groups on the basis of growth habit (e.g., P'ei, 1935
; Huang, 1977
; Wu, 1982
; Lin, 2000
).
Recently, however, evidence from cytology and comparative anatomy indicated that in Chloranthus the boundary between the herbaceous species and the suffrutescent ones is unclear. Cytologically, species of Chloranthus could be divided into two distinctly different groups according to their karyotypes, especially the size and shape of the first eight (or 16 in tetraploid species) chromosomes. In C. angustifolius, C. fortunei, C. nervosus, and C. japonicus (the only four species of sect. Macronuri with a herbaceous habit and long androecial lobes), these chromosomes are all median-centromeric (m-type), while in C. erectus, C. spicatus (the only two species of sect. Triandri with a suffrutescent habit and short androecial lobes), C. serratus, and C. sessilifolius (two species of sect. Brachyuri with herbaceous habit and short androecial lobes), they are median-, submedian- (sm-type), or even subterminal-centromeric (st-type) (Hizume and Tanaka, 1982
, 1988
; Kong, 2000b
). Anatomically, fibre-tracheids were found to be present in stems of C. erectus, C. spicatus, C. serratus, C. sessilifolius, and C. henryi, but absent in those of C. angustifolius, C. fortunei, C. nervosus, and C. japonicus (Carlquist, 1992
; H.-Z. Kong, unpublished data). Studies on the leaf epidermis of Chloranthaceae also revealed that paracytic stomata predominate in sections Triandri and Brachyuri, while laterocytic ones predominate in sect. Macronuri (Kong, 2001
). All this seems to suggest that the infrageneric phylogeny of Chloranthus needs to be reconsidered.
In order to better understand relationships and character evolution within Chloranthaceae, Eklund (1999)
conducted a cladistic analysis on living and fossil taxa of the family, using 107 morphological characters. The results indicated that the family Chloranthaceae and the four extant genera (Sarcandra, Chloranthus, Ascarina, and Hedyosmum) are all monophyletic groups. Within Chloranthus, C. spicatus was resolved as the first branching species, followed by C. erectus, C. serratus, C. anhuiensis, C. oldhamii, C. nervosus, C. fortunei, C. angustifolius, and C. japonicus (Eklund, 1999
; Analysis I). From these results, it is evident that none of the previous treatments in Chloranthus is reasonable and that neither growth habit nor androecium morphology can act as the primary character to delimit Chloranthus species.
Considering that the results of Eklund (1999)
differ significantly from those of the morphological, anatomical, and cytological studies mentioned above and that the relationships among species are of utmost importance in discussing the evolutionary trends of character states, DNA sequence data were included to evaluate the phylogeny of Chloranthus. In this study, portions of two genomes were used, i.e., the internal transcribed spacers (ITS) of the nuclear ribosomal DNA and the trnL-F region from the chloroplast DNA. As shown in Kong and Chen (2000)
, ITS sequences can provide valuable information in understanding the relationships among species of Chloranthus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DNA extraction, amplification, and sequencing
Total DNA was isolated from fresh or silica-dried leaves using the cetyltrimethylammonium bromide CTAB method described by Doyle and Doyle (1987)
and purified with a Wizard DNA Clean-up system (Promega, Madison, Wisconsin, USA). Primers "ITS5" and "ITS4" (White et al., 1990
) were used to amplify ITS-1, 5.8S rDNA, and ITS-2 of the ITS region, and "c" and "f" (Taberlet et al., 1991
) to amplify the intron, 3' exon, and the intergenic spacer of the trnL-F region. The ITS region was amplified using the polymerase chain reaction (PCR) conditions described by Kong and Chen (2000)
. For trnL-F region, double-stranded DNA amplications were performed in a 20-µL volume containing 9.5 µL of sterile distilled water, 2.5 µL of 200 µmol/L dNTPs in equimolar ratio, 2.5 µL of 10x Taq DNA Polymerase buffer (Promega), 2.5 µL 25 mmol/L MgCl2, 0.5 µL each of 10 mmol/L primer, 0.5 units of Taq DNA Polymerase (Promega), and 2 µL of genomic DNA (1–10 ng). The temperature profile for amplication of trnL-F region consists of initial denaturation at 94°C for 3 min, followed by 32 cycle of denaturation (94°C for 1 min), annealing (48°C for 1 min), and extension (72°C for 3 min), with a final extension at 72°C for 7 min. Polymerase chain reaction was conducted in a thermocycler (Perkin Elmer 9600, Norwalk, Connecticut, USA), and the PCR products were purified using Wizard PCR preps DNA Purification System (Promega), following the manufacturer's instructions. After sequencing reactions were performed with PRISM Dye Terminator Cycle Sequencing Ready Reaction kits (Perkin-Elmer Applied Biosystems, Norwalk, Connecticut, USA), sequencing products were electrophoresed and analyzed automatically using an ABI 377 automated DNA Sequencer.
Data analysis
The ITS and trnL-F region boundaries were determined by comparison with sequences available in GenBank. All sequences were aligned manually, and phylogenetic analyses were performed using PAUP version 3.1.1 (Swofford, 1993
). Data were initially analyzed as separate ITS and trnL-F sets. Since the ITS tree does not differ much from the trnL-F tree, we have combined the two matrices directly in spite of the lack of tests for combinability of them. All transformations were unordered and weighted equally in both data sets (Fitch parsimony; Fitch, 1971
); gaps were coded as missing values. For each analysis (ITS, trnL-F, and combined), 100 replications of random addition were conducted using heuristic searches with tree-bisection-reconnection (TBR) branch-swapping and the MULPARS option to save all most parsimonious trees. Bootstrap analyses were conducted using 1000 resampling replicates with the random addition and heuristic search options.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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When sequences from all taxa of Chloranthus and the outgroup Sarcandra glabra were considered with gaps treated as missing data, one most parsimonious tree of 84 steps was recovered (Fig. 2). The CI and RI were 0.964 and 0.941, respectively. Two well-supported clades, one (Clade A) containing C. erectus, C. spicatus, C. serratus, C. henryi, C. sessilifolius, and C. oldhamii and the other (Clade B) including C. angustifolius, C. fortunei, C. nervosus, and C. japonicus, were formed. Within Clade A, two subclades were also recognizable: one of C. erectus and C. spicatus and the other of C. serratus-C. henryi and C. sessilifolius-C. oldhamii.
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The analysis based upon the combined data sets echoes the results found in the separate analyses, but with stronger level of bootstrap support. This analysis yielded one most parsimonious tree (Fig. 3), 311 steps long, with a CI of 0.826 and an RI of 0.702. The topology is the same as that based on trnL-F data, and the bootstrap values of the two clades are 94% and 98%. Within Clade A, two well supported small clades, one containing C. erectus and C. spicatus and the other C. serratus-C. henryi and C. sessilifolius-C. oldhamii, were apparent.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Eklund, 1999
; Qiu et al., 1999
, 2000
; Mathews and Donoghue, 2000
; Soltis et al., 2000
), while the delimitation between these two genera is still unclear (e.g., Solms-Laubach, 1869
; Bentham and Hooker, 1880
; Nakai, 1930
; P'ei, 1935
; Swamy and Bailey, 1950
; Swamy, 1953
). Nakai (1930)
advocated a separation of Sarcandra from Chloranthus, and his point of view was accepted by many of the following researchers (e.g., Swamy and Bailey, 1950
; Swamy, 1953
; Endress, 1987
; Crane, Friis, and Pedersen, 1989
; Todzia, 1993
; Eklund, 1999
). According to the studies of Swamy and Bailey (1950)
, Sarcandra is clearly distinguished from Chloranthus by its unique characteristics such as the bisexual flowers with a single stamen, orange to red fruits, vesselless xylem, and acolpate pollen grains. Decades later, however, vessels were repeatedly reported in both the stems and roots of S. glabra and S. hainanensis (Carlquist, 1987
; Takahashi, 1988
; Takahashi and Tamura, 1990
; Zhang et al., 1990
), and apertures were found in the pollen grains of Sarcandra (Kuprianova, 1967
; Endress, 1986
, 1987
). Chloranthus serratus and C. henryi have a tripartite androecium early in the flowering season, but a bipartite or single androecium later (Wang, Huang, and Wu, 1984
; Kong, 2000a
). All this seems to narrow the gap between these two genera.
More recently, evidence from cytological and anatomical studies revealed several differences between these two genera (Hizume and Tanaka, 1982
; Okada, 1995
; Kong, 2000b
, 2001
). Cytologically, the interphase nuclei and prophase chromosomes of Sarcandra are of the complex chromocenter type and the interstitial type, while those of Chloranthus are of the prochromosome type and the proximal type (Hizume and Tanaka, 1982
; Okada, 1995
). At metaphase, the first four pairs of chromosomes of the species in Sarcandra are all subterminal-centromeric chromosomes, with a pair of large satellites located on the short arms of the third pair of chromosomes; these eight chromosomes, together with the two large satellites, may serve as a marker, by which species in Sarcandra are cytologically distinguishable from those in Chloranthus (Kong, 2000b
). Species of Sarcandra also differ from those of Chloranthus in some features of leaf epidermis (Kong, 2001
). In Sarcandra, encyclocytic, incompletely encyclocytic, and a few paracytic stomata occur along with the predominant laterocytic ones, and the outer stomatal rims are almost level with the epidermis, while in Chloranthus neither encyclocytic nor incomplete encyclocytic stomata can be observed (except for 3.1% in C. serratus), and the outer stomatal rims are always prominently raised.
In the present study, species of Sarcandra show somewhat great differences from those of Chloranthus in DNA sequences. In the ITS region, for example, 47 sites, 22 (or 19.2%) in ITS-1 and 25 (or 11.7%) in ITS-2, supported the separation of Sarcandra from Chloranthus, and the sequence divergences are 0.8% to 9.0% among species of Chloranthus, and 11.5% to 15.8% between Chloranthus and Sarcandra. When the gaps were treated as missing, one most parsimonious tree with Sarcandra and Chloranthus as two major clades was obtained. Similar results were also found when trnL-F and combined data sets were included in the analysis. Thus, our analyses supported the separation of these two genera.
Phylogenetic relationships within Chloranthus
Parsimony analyses based on ITS and trnL-F sequences strongly suggest that Chloranthus can be divided into two major clades (Figs. 1–3): one containing C. erectus, C. spicatus, C. serratus, C. henryi, C. sessilifolius, and C. oldhamii (Clade A) and the other comprising C. angustifolius, C. fortunei, C. nervosus, and C. japonicus (Clade B). Species of Clade A are characterized by their tripartite androecium with short connectives, while those of Clade B have a tripartite androecium with distinctly long connectives. Taxonomically, these two clades correspond to Bentham and Hooker's (1880)
sections Euchloranthus and Tricercandra, respectively.
Chloranthus erectus and C. spicatus were resolved as paraphyletic in the ITS tree (Fig. 1), while in the trees that resulted from trnL-F and combined data sets (Figs. 2, 3), they formed a well-supported monophyletic group. Considering that C. erectus and C. spicatus also share such morphological and anatomical features as a suffrutescent habit, 10- to 20-spiked inflorescences, shell-shaped androecia with three lobes almost completely united, and entirely paracytic stomata in the leaf epidermis (Wu, 1982
; Verdcourt, 1986
, 1992
; Kong, 2000a
, 2001
), we hold that Solms-Laubach's (1869)
sect. Triandri is a monophyletic group, instead of a paraphyletic one as Eklund (1999)
supposed.
From this study, it is clear that many of the previous infrageneric ranks in the genus Chloranthus, such as sections Triandri, Brachyuri, and Macronuri of Solms-Laubach (1869)
and Euchloranthus and Tricercandra of Bentham and Hooker (1880)
, were all resolved as monophyletic groups. Solms-Laubach's subgenera Fruticosi and Herbacei, however, were resolved as paraphyletic. So the traditional division of the genus Chloranthus on the basis of habit was not supported. Evidence from molecular sequences, in agreement with that from morphology (Kong, 2000a
), anatomy (Carlquist, 1992
; Kong, 2001
), and cytology (Kong, 2000b
), strongly supported the viewpoint that Chloranthus consists of two groups that morphologically may be distinguished by their androecial characters.
Evolution of the androecia of Chloranthus
The androecium of Chloranthus is generally a three-lobed structure with four thecae (Fig. 3; Swamy, 1953
; Endress, 1987
). The androecia of C. henryi, C. sessilifolius, and C. oldhamii are slightly reflexed apart from the spike axis, with three androecial lobes united only at the base. The androecium of C. serratus, however, forms a small scale-like structure and exhibits an early step in the cohesion of the adjacent lobes. This tendency finds an extreme expression in the androecium of C. erectus and C. spicatus; in these two species, the androecial lobes are strongly involute and almost wholly coherent (Swamy, 1953
; Endress, 1987
; Kong, 2000a
). Most importantly, the androecial lobes of all the aforementioned species are very short, while those of C. angustifolius, C. fortunei, C. nervosus, and C. japonicus are elongated, with the confluent base rather pronounced (Swamy, 1953
; Endress, 1987
).
Whether the androecial structure of Chloranthus represents a single stamen with four pairs of sporangia or three independent stamens that have undergone fusion at the base has long been controversial (Swamy, 1953
; Endress, 1987
; Crane, Friis, and Pedersen, 1989
; Herendeen, Crepet, and Nixon, 1993
; Zhou, 1993
; Eklund, Friis, and Pedersen, 1997
; Eklund, 1999
). The stamen has been described as "a single stamen," "three stamens," "three anthers," "a single tripartite anther," or "a three-lobed filament" (see Swamy, 1953
). Two hypotheses were also proposed to interpret its evolutionary origin: it may have evolved from three stamens by loss of the inner thecae of each lateral stamens, or it may have originated from a single stamen by fractionation of the thecae into an upper and a lower part on both sides (Swamy, 1953
; Endress, 1987
; Eklund, 1999
). Based mainly on the mesofossil evidence from paleobotanical studies, the majority of researchers preferred to regard it as being composed of three individual stamens (Crane, Friis, and Pedersen, 1989
; Herendeen, Crepet, and Nixon, 1993
; Zhou, 1993
; Eklund, Friis, and Pedersen, 1997
), while Endress (1987)
inclined to consider it as a single tripartite stamen. Eklund (1999)
, who had conducted a phylogenetic analysis on the Chloranthaceae using neobotanical and paleobotanical data, made a summary on the hypotheses for the origins of the three-lobed androecium in Chloranthus and concluded that it might have originated by fusion of three independent stamens. Unfortunately, Eklund's point of view was not supported even by her own cladistic analyses, because the species with androecial lobes coherent at the base (e.g., C. oldhamii) were resolved as a later-branching species within Chloranthus.
In our combined molecular tree, species with androecial lobes united only at the base (i.e., C. henryi, C. sessilifolius, and C. oldhamii) are nested within the clade formed by species with androecial lobes united to a higher degree (Figs. 1–3). Considering that the hexaploid C. henryi still possesses a close affinity to the diploid C. serratus and that Chloranthus-like plants with androecial structures resembling those of C. erectus, C. spicatus, and C. serratus were well established in the Turonian of the Later Cretaceous (e.g., Chloranthistemon crossmanensis Herendeen, Crepet and Nixon), we concluded that in this genus the androecia with three lobes united only at the base may be an apomorphic character state and that the androecial structure of Chloranthus may have arisen by splitting of a single stamen with two marginal thecae. Figure 4, adopted and modified from Endress (1987)
, could well illustrate our present understanding of the evolution of androecial structure in Chloranthus.
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FOOTNOTES |
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2 Author for reprint requests (hongzhi_kong{at}hotmail.com
)
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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 Dark and disturbed: a new image of early angiosperm ecology Paleobiology, January 1, 2004; 30(1): 82 - 107.
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, perennial herb