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0 Biological Institute, Graduate School of Science, Tohoku University, Sendai, 980-8578 Japan
Received for publication April 20, 1998. Accepted for publication May 4, 1999.
ABSTRACT
Nucleotide sequences of the chloroplast-encoded rbcL gene were used to examine phylogenetic relationships of the genus Salix together with other allied genera of the family Salicaceae. Phylogenetic analyses of rbcL sequences strongly suggest the monophyly of three commonly recognized genera (Chosenia, Salix, and Toisusu). Two monophyletic groups are recognized within the larger monophyletic group. They do not correspond with any infrageneric taxa proposed so far. With regard to character evolution, it is thought that the reduction of stamen number from more than two stamens to two might occur in at least three lineages and that fused bud scales evolved several times and/or the reverse evolution occurred from fused to free. Some types of pollen surfaces are considered to have evolved independently.
Key Words: Chosenia • cpDNA • rbcL • Salicaceae • Salix • taxonomic treatments • Toisusu
Salix L. is by far the largest of the 2–4 genera of the family Salicaceae. Systematic treatments of Salix have varied extensively (Table 1). Salicaceae was divided into Salix and Populus when it was originally described by Linnaeus (1753). Nakai (1920)
segregated a new genus Chosenia Nakai based on Salix splendida Nakai because of its anemophilous flowers, pendulous aments, and bud scales free adaxially. Kimura (1928)
established a new genus Toisusu Kimura based on three species of Salix that have pendulous aments, free bud scales, and deciduous bifid styles. On the other hand, Skvortsov (1968)
included Toisusu in Salix because its diagnostic characters (e.g., pendulous aments and deciduous styles) are also found in some other species of Salix.
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divided Salix into two subgenera, and Skvortsov (1968)
into three. Later, Kimura (1988)
returned Chosenia and Toisusu as Salix subg. Pleuradenia Kimura. Such taxonomic discordance in systems of Salix at the generic and subgeneric level are caused by scarceness of informative morphological characters that can be used for systematic studies. Although many important characters for systematics of angiosperms are chiefly obtained from flowers, such floral characters are limited in Salicaceae because of their extremely reduced flowers. It is necessary, therefore, to seek other sources of information for reexamining the classification of Salix.
Macromolecular characters such as nucleotide sequences of DNA or amino acid sequences of proteins are frequently used today to reconstruct phylogenetic relationships of various kinds of organisms. In Salicaceae, Smith and Sytsma (1990)
analyzed restriction fragment length polymorphisms (RFLPs) of cpDNA and nrDNA to examine phylogenetic relationships within the genus Populus. However, they worked only on Populus and did not discuss Salix. The only published molecular systematic work in Salix is a study of cpDNA RFLPs that aimed to examine phylogenetic relationships of Salix sect. Longifoliae Pax (Brunsfeld, Soltis, and Soltis, 1992
). The phylogenetic relationships they obtained did not agree with taxonomic concepts based on morphological characters. Their work was restricted to sect. Longifoliae and did not discuss classification for the entire range of the genus Salix. Therefore, we should examine the entire range of Salix using macromolecular characters.
We performed phylogenetic analyses based on nucleotide sequences of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL). RbcL has been used for phylogenetic analyses in a wide range of angiosperms (e.g., Chase et al., 1993
; Conti, Fischbach, and Sytsma, 1993
; Morgan and Soltis, 1993
; Price and Palmer, 1993
; Xiang et al., 1993
; Bremer, Andreasen, and Olsson, 1995
; Olmstead and Reeves, 1995
). In this paper, we examined the following two points: (1) whether or not Chosenia and Toisusu are phylogenetically distinct from Salix and (2) which system of Salix may be best supported by our phylogenetic analyses.
MATERIALS AND METHODS
We selected 23 species from four genera of Salicaceae (Table 2), including species from all sections of Salix subg. Salix (sensu Skvortsov, 1968
): sect. Amygdalinae Koch, sect. Glandulosae Kimura, sect. Humboldtianae Pax, sect. Longifoliae Pax, sect. Pentandrae (Borrer) Schneid., sect. Salix and sect. Subalbae Koidz. In Salix subg. Chamaetia (Dumortier) Nasarov and Salix subg. Vetrix Dumortier (sensu Skvortsov, 1968
), we selected species whose morphology and distribution are quite different from each other. Voucher specimens of all materials are deposited in the Herbarium, Biological Institute, Graduate School of Science, Tohoku University (TUS).
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as modified by Doyle and Doyle (1987)
. Most DNA samples were obtained from fresh leaf materials, but five samples were from herbarium specimens. The rbcL gene was amplified from total DNA via the polymerase chain reaction (PCR; Saiki et al., 1988
) using the "universal" primers provided by G. Zurawski (DNAX Corporation; described in Zurawski et al., 1981
; Zurawski, Whitfeld, and Bottomley, 1986
; Table 3). Amplification was carried out in 50 µL of reaction solution containing 10–20 ng of genomic DNA, 20 pmol/L (each) amplification primers, 10 nmol/L dNTP, 50 mmol/L KCl, 1.5 mmol/L MgCl2, 10 mmol/L Tris-HCl (pH 9.0), and 1.25 units of Taq DNA polymerase (Pharmacia Biotech, Tokyo, Japan). A TSR-200 Thermal Sequencer (Iwaki Glass Co., Tokyo, Japan) with the following cycles were used for amplification of particular portions of the rbcL gene: 1 min at 94°C followed by 30 cycles of 1 min at 94°C, 1.5 min at 56°C, and 2 min at 72°C. The final cycle was followed by an extension step of 15 min at 72°C.
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Because Salicaceae was not included in the global analysis of angiosperm phylogeny by Chase et al. (1993)
, it was necessary to first determine the sister group of Salicaceae to obtain an appropriate outgroup for subsequent analyses. To determine the sister group of Salicaceae, phylogenetic analyses were performed using 16 additional rbcL sequences selected from the ENBL/GenBank/DDBJ database (Table 4). Candidates for the sister group were chosen from previous angiosperm classification systems: Betula L., Casuarina Adans., Carya Nutt., Fagus L., and Myrica L. in Amentiferae sensu Engler (1894); Daphniphyllum Blume, Hamamelis L., Platanus L., and Tetracentron Oliv. in Hamamelidales sensu Hutchinson (1964)
; Passiflora L., Viola L., and Begonia L. in Violales sensu Cronquist (1988)
. All of these groups are included in the rosid or the hamamelid clade of Chase et al. (1993)
. Euphorbia L., which was included in the rosid clade of Chase et al. (1993)
, was also included in the analysis. The sequence of Idesia Maxim., which is considered to be close to Salicaceae (Meeuse, 1975), was determined in this study (Table 2) and included in the analysis. Muntingia L. and Dovyalis E. May, the other published sequences of Flacourtiaceae, were also included in the analysis. The sequence of Ranunculus L., which was included in the ranunculids of Chase et al. (1993)
, was selected as the outgroup. The sequences of Populus maximowiczii A. Henry (this study, Table 2) and Salix sachalinensis Fr. Schm. (this study, Table 2) were selected as representatives of Salicaceae.
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Parsimony analyses were performed using PAUP version 3.1.1 (Swofford, 1993
) with all changes weighted equally. To find multiple islands of most parsimonious trees (Maddison, 1991
), 100 random order entry replication searches were employed in each analysis. HEURISTIC searches of TBR and NNI branch swapping option were used for the analyses. Neighbor-joining (NJ) analyses were performed using NEIGHBOR in PHYLIP version 3.57 (Felsenstein, 1993
). Sequence divergence values were calculated by Kimura's two-parameter method (Kimura, 1980
) using DNADIST in the same package. In both methods, the statistical confidence level of each branch was estimated by the bootstrap method (Felsenstein, 1985
). In NJ analyses, bootstrap analyses were performed using SEQBOOT in the same package.
RESULTS
Phylogenetic position of the Salicaceae
In the analysis to determine the sister group of the Salicaceae, a single most parsimonious trees was obtained by parsimony analyses with both branch swapping options (length = 689, consistency index [CI] excluding uninformative sites = 0.534, rescaled consistency index [RC] = 0.350; Fig. 1). The Salicaceae were a monophyletic group, and the monophyly was statistically supported (bootstrap value: 65%). Among the putative related groups, Idesia was the most closely related taxa to Salicaceae and Dovyalis followed. The monophyly of this clade was supported with high bootstrap value (100%). In the tree obtained from neighbor-joining analyses (Fig. 2), the monophyly of Salicaceae was supported (bootstrap value: 63%) and its sister-group relationship with Idesia and Dovyalis was also supported with high confidence level (100%). Based upon these results, phylogenetic analyses within Salicaceae were undertaken using Idesia and Dovyalis as the outgroup.
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Within clade 2, Salix bebbiana Sargent, S. discolor Muhlenberg, S. hastata L., S. integra Thunb. ex Murray, S. kirilowiana Stschegl., S. reinii Franch. et Savat., S. reticulata L., S. sachalinensis, and S. subreniformis Kimura formed a monophyletic group with high confidence level (92%). This monophyletic group formed a trichotomy with Chosenia arbutifolia and Toisusu urbaniana. Salix subfragilis came at the basal position of clade 2. No differences were found between the sequences of C. arbutifolia and T. urbaniana. There were also no differences among the sequences of Salix bebbiana, S. discolor, S. hastata, S. integra, S. kirilowiana, S. reinii, S. reticulata, S. sachalinensis, and S. subreniformis.
The same result was obtained by the neighbor-joining analyses on Salicaceae (Fig. 4). However, loss of information through calculating sequence divergence values caused low statistical supports of particular branches, because sequence divergences among species of Salix are very low (0–0.079 in clade 1, and 0–0.058 in clade 2, calculated by Kimura's two-parameter method). Since parsimony analyses can reconstruct the true phylogenetic relationship in such case of low genetic divergences (Sourdis and Nei, 1988
), phylogenetic relationships within Salicaceae were discussed based on the tree obtained by the maximum parsimony method.
DISCUSSION
Phylogenetic position of the Salicaceae
In our analysis Idesia and Dovyalis of Flacourtiaceae are the sister groups of the Salicaceae. According to Nandi, Chase, and Endress (1998)
, Flacourtiaceae, together with Scyphostegiaceae, became also the sister group of Salicaceae in the global analyses of angiosperm phylogeny using rbcL and in the combined analyses using rbcL and non-molecular data set. Our molecular data congruent with their results on close relationships between Flacourtiaceae and Salicaceae.
Generic placement of Chosenia and Toisusu
Chosenia and Toisusu are often divided from Salix at the generic level because of their pendulous aments and bud scales free at adaxial side like Populus (Table 1). In our molecular analyses, however, the monophyly of clade 2, with a high bootstrap value (93%), indicates that Chosenia and Toisusu cannot be divided from Salix as distinct genera. Thus there is no evidence that Chosenia and Toisusu are closer to Populus than to Salix. The placement of Chosenia and Toisusu in the genus Salix is in agreement with the generic assignments of Kimura (1988)
. However, we use the names Chosenia and Toisusu to avoid confusion in following discussions.
Kimura (1938, 1988)
considered Chosenia to be closely allied with Toisusu on the basis of the fact that Chosenia sometimes has vestiges of glands in the same position as in Toisusu. In our molecular data, however, these two taxa form a trichotomy with the clade that consisted of Salix subg. Chamaetia and subg. Vetrix (Fig. 5). Therefore, to further examine the relationship of Chosenia and Toisusu, we should use genes that have higher rate of sequence evolution than rbcL.
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suggested a close relationship between Toisusu (as sect. Urbanianae (Seem.) Schneid. of Salix sensu Skvortsov, 1968
) and Salix subg. Vetrix based on anatomical characters of the leaves. In species of Toisusu and Salix subg. Vetrix, a hypodermis is not found in either side of the leaf. He also reported that Salix sect. Longifoliae, to which S. interior belongs, has a specific leaf character and is considered to be similar to Chosenia. Salix sect. Longifoliae and Chosenia have a hypodermis that lacks chloroplasts in both sides of the leaf, while this leaf structure is not found in species of other sections of Salix (Skvortsov, 1968
). In our molecular data (Fig. 5), the monophyly of clade 2, which contains Toisusu and Salix subg. Vetrix, suggests a close relationship between Toisusu and Salix subg. Vetrix and supports his view of their relationship. This proposed relationships between S. interior and C. arbutifolia, however, is not supported by our data, since each of them belongs to a different clade (S. interior in clade 1, and C. arbutifolia in clade 2). Thus, the leaf character outlined is considered to have evolved independently.
Erdtman (1966)
reported that pollen grains of Populus are nonaperturate and those of Salix are three-colporoidate. Sohma (1993)
reported that palynologically there is no difference among Chosenia, Toisusu, and Salix and concluded that pollen studies support merging Chosenia and Toisusu into Salix. In our molecular data (Fig. 5), the members of Salix other than Chosenia and Toisusu are paraphyletic. Therefore, our molecular data support this viewpoint.
Phylogenetic relationships of Salix
This study revealed that there are two clades in Salix. We compared these two clades with taxonomic systems proposed so far. Andersson (1868) divided Salix into three groups mainly based on stamen characters: Pleiandrae Anderss, which has more than two stamens (but S. alba and S. babylonica included in this group have two stamens), Diandrae Anderss, which has two separate stamens, and Synandrae Anderss, which has two connate stamens. Our molecular tree suggested that Pleiandrae were paraphyletic and Diandrae were polyphyletic and that Synandrae formed a monophyletic group with most of Diandrae except for S. interior (Fig. 5).
With regard to stamens, Skvortsov (1968)
considered that the reduction of stamen number from more than two stamens to two might occur in three lineages, yielding the following three groups: (1) Salix sect. Longifoliae, (2) Salix sect. Salix and sect. Subalbae Koidz., and (3) Salix subg. Chamaetia and subg. Vetrix. In our molecular data (Fig. 5), subg. Chamaetia and subg. Vetrix formed a monophyletic group, while S. babylonica f. rokkaku of sect. Subalbae and S. alba of sect. Salix appeared in another clade, though they formed a trichotomy with S. pentandra, which has more than two stamens. These two groups and S. interior of sect. Longifoliae, the third two-stamen group, appeared independently. Therefore, our molecular data support Skvortsov's viewpoint concerning the evolution of stamens.
Kimura (1928)
divided Salix into two subgenera, Protitea Kimura, which has free bud scales, and Euitea Kimura, which has fused ones. In our phylogenetic tree (Fig. 5), members of Euitea appeared several times independently in different clades. Therefore, it is possible that fused bud scales evolved several times and/or the reverse evolution occurred from fused to free.
Skvortsov (1968)
included Toisusu in Salix and recognized three subgenera in the genus (Table 1). In his system, members of subg. Salix have at least one character that was considered to be primitive (e.g., more than two stamens, free bud scales), while subg. Chamaetia and subg. Vetrix mainly have characters presumed to be advanced (e.g., two stamens, fused bud scales). Subgenus Chamaetia comprises species that are repent and have terminal aments. They are considered to be adaptive to arctic and alpine climates. Subgenus Vetrix consists of the remainding advanced Salix species. In our cladogram (Fig. 5), subg. Salix in his scheme is paraphyletic. Although subg. Chamaetia and subg. Vetrix form a monophyletic group, the monophyly of each subgenus is unresolved, because sequences obtained from both subgenera are identical.
In our tree, tetraploid (2n = 76) species, represented by Salix babylonica f. rokkaku, S. alba, and S. pentandra, are supported as a monophyletic group. Suda (1963)
grouped sections of Salix into six groups based on chromosome numbers (Fig. 5), and these three species were included in his third group, which were tetraploid (2n = 76) and hexaploid (2n = 114). Therefore, our molecular data support his third grouping. Salix subfragilis, which was included in his second group (which consists of species whose chromosome number are 2n = 38 and 44), came at the basal position of clade 2 in this study. He regarded this second group as being cytologically intermediate between his first group and other groups. In our result, however, there is no evidence that his second group is close to his first group or other groups. His first group, which consists of only diploid (2n = 38) taxa, is separated into two groups. With respect to the other groups, however, we cannot discuss them because phylogenetic relationships within these groups are unresolved.
Sohma (1993)
examined pollen grains of 72 taxa of Salix and divided them into eight types based on reticulate patterns of pollen surfaces. When the subdivision of pollen types is compared with the results of this study, types 1, 2, 4, 5, and 6 of Sohma are distributed in both clades 1 and 2 (Fig. 5). Therefore, our molecular data suggest that some types of pollen surfaces evolved independently.
Recently, Argus (1997)
made a phenetic analysis of Salix in the New World and Chosenia and established a new system. He grouped Chosenia with Salix subg. Salix, though in the present study it is grouped with S. subg. Vetrix. One of the reasons for the discordance between his results and ours may be differences of analyses. Further analyses of both morphological and molecular data are needed to confirm the phylogenetic relationships of these groups.
We cannot discuss other Salix systems, e.g., Koch (1828), Fries (1832)
, Seemen (1903)
, Schneider (1916)
, Hao (1936)
, Rehder (1949)
, because species treated in their systems were limited, materials used in this study were not comparable, and our results could not resolve the problems at the species level. We should reexamine these systems using more species and using genes that have higher rate of sequence evolution than rbcL.
No morphological, anatomical, palynological, or cytological characters that support the two phylogenetic groups of Salix obtained in our results were found in any previous studies. Therefore, we should examine Salix for additional characters suggesting phylogenetic relationships.
We demonstrated using cpDNA that there are two clades in Salix. However, extensive hybridization is known and cytoplasmic capture has been discovered in the Salicaceae (Brunsfeld, Soltis, and Soltis, 1992
). Thus, it is probably difficult to discuss the exact history of evolution by using cpDNA alone. Therefore, we should also examine nuclear markers like nrDNA to reveal the history of evolution in the Salicaceae.
In this study, we achieved extensive phylogenetic knowledge of the Salicaceae using the rbcL gene. Our results alone do not reveal the evolution of the Salicaceae, and it is necessary to examine other molecular sources to confirm the results of this study.
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1 The authors thank Drs. M. W. Chase and G. Zurawski for providing information on sequencing primers, Drs. S. Sugaya, H. Tohda, Mr. H. Nakai, and Mr. M. Yashima for help in obtaining plant materials; Drs. A. Kimura, K. Sohma, M. Suzuki, T. Nemoto, H. Sakai, and W.-G. Park for helpful discussion; Dr. D. E. Boufford for reading the manuscript; and Dr. G. W. Argus for constructively reviewing our manuscript. 
2 Current address: Botanical Gardens, Faculty of Science, University of Tokyo, 3-7-1 Hakusan, Bunkyo-ku, Tokyo, 112 Japan.
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