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1 Section of Evolution and Ecology, University of California, Davis, California 95616 USA; 2 Department of Plant Science, Montana State University, Bozeman, Montana 59717 USA; and 3 Museum of Paleontology and University/Jepson Herbaria, University of California, Berkeley, California 94720 USA
Received for publication March 5, 1999. Accepted for publication June 22, 1999.
ABSTRACT
Phylogenetic relationships in the tribe Millettieae and allies in the subfamily Papilionoideae (Leguminosae) were reconstructed from chloroplast trnK/matK sequences. Sixty-two accessions representing 57 traditionally recognized genera of Papilionoideae were sampled, including 27 samples from Millettieae. Phylogenies were constructed using maximum parsimony and are well resolved and supported by high bootstrap values. A well-supported "core Millettieae" clade is recognized, comprising the four large genera Millettia, Lonchocarpus, Derris, and Tephrosia. Several other small genera of Millettieae are not in the core Millettieae clade. Platycyamus is grouped with Phaseoleae (in part). Ostryocarpus, Austrosteenisia, and Dalbergiella are neither in the core Millettieae or Phaseoleae clade. These taxa, along with core Millettieae and Phaseoleae, form a monophyletic sister group to Indigofereae. Cyclolobium and Poecilanthe are close to Brongniartieae. Callerya and Wisteria belong to a large clade that includes all the legumes that lack the inverted repeat in their chloroplast genome, which confirms previous rbcL and phytochrome gene family phylogenies. The evolutionary history of four characters was examined in Millettieae and allies: the presence of canavanine, inflorescence types, the dehiscence of pods, and the presence of winged pods. trnK/matK sequence analysis suggests that the presence of a pseudoraceme or pseudopanicle and the accumulation of nonprotein amino acids are phylogenetically informative for Millettieae and allies with only a few exceptions.
Key Words: Fabaceae • matK • Millettieae • Papilionoideae • phylogeny • trnK.
Leguminosae (Fabaceae) is one of the largest families of flowering plants, comprising over 650 genera and 18000 species (Polhill, Raven, and Stirton, 1981
). The predominantly tropical tribe Millettieae, consisting of over 40 genera and nearly 1000 species, is generally thought to have given rise to many temperate herbaceous groups and several tropical tribes of papilionoid legumes, such as Phaseoleae, Indigofereae, Galegeae, and their allies (Polhill, 1981
; Geesink, 1984
). The circumscription of this tribe is vague, i.e., tropical woody papilionoids with derived flower features (fused keel petals), wood with conspicuously banded parenchyma (Baretta-Kuipers, 1981
), and seeds containing nonprotein amino acids, but there are many exceptions (Polhill, 1981
; Lavin et al., 1998
). The tribe is traditionally divided into three subgroups, with Tephrosia, Millettia, and Derris as the major components in each (Geesink, 1984
). Derris and allies (e.g., Lonchocarpus) have been placed in the tribe Dalbergieae because of indehiscent pods (Bentham, 1860
). Millettia and Tephrosia, with dehiscent pods, were separated from Derris and Lonchocarpus, and have been placed within a broadly circumscribed tribe Galegeae (Bentham, 1865
), or in the more narrowly circumscribed tribe Tephrosieae (Gillett, 1971
). Geesink (1981)
established Millettieae (formerly Tephrosieae s.l. [sensu lato]) and included all the genera mentioned above. He noted a possible transition from Dalbergieae, through Derris/Lonchocarpus and Millettia/Tephrosia, to Galegeae. Galegeae was thought to be the "connection" between Millettieae and all the other temperate herbaceous groups in Papilionoideae (Polhill, 1981
).
A survey of the 25-kb inverted repeat (IR) in the chloroplast genome of legumes (Lavin, Doyle, and Palmer, 1990
; Liston, 1995
) revealed a presumably monophyletic group that lost the IR. It includes the temperate tribes Galegeae, Carmichaelieae, Cicereae, Hedysareae, Vicieae, and Trifolieae, as well as several species from Millettieae, i.e., Wisteria, Millettia japonica, and the tropical genus Callerya, which we designate as the IR-lacking clade ("IRLC"; see Fig. 1). The monophyly of this IR-lacking clade is supported by rbcL data (Doyle et al., 1997
) and phytochrome gene family studies (Lavin et al., 1998
). However, Wisteria and Callerya have a very similar appearance to Millettia and several other Millettieae (Geesink, 1984
; Zandee and Geesink, 1987
). One goal of the present study was to verify the pattern of the loss of IR with more intensive sampling for Millettieae and to explore the implications of these data.
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) or phytochrome gene family trees (Lavin et al., 1998
). It is probable that rbcL is evolving too slowly, and it is difficult to rule out the potential problems of orthology in phylogenies constructed from multigene families (i.e., phytochrome data) (Sanderson and Doyle, 1992
). Therefore, we use another chloroplast region, trnK/matK (including the trnK intron), which has been used successfully in phylogenetic studies at the generic level in the families Polemoniaceae and Apiaceae (Steele and Vilgalys, 1994
; Plunkett, Soltis, and Soltis, 1996
), to reconstruct the phylogeny of the tribe Millettieae.
The pattern of character evolution was examined in four morphological characters: the presence of canavanine (a nonprotein amino acid unique in higher Papilionoideae), inflorescence types, presence of wing(s) on the pods, and dehiscence of the pods. These characters have been important for distinguishing Millettieae from other tribes (Polhill, 1981
) and in diagnosing genera within Millettieae (Geesink, 1984
). The distribution of character states was determined from the descriptions of Millettieae in Geesink (1984)
, and Polhill and Raven (1981)
, and superimposed on the trnK/matK phylogeny.
MATERIALS AND METHODS
Sampling materials and total DNA extraction
The sampling in this study includes 27 Millettieae species and the taxa from Papilionoideae considered to be closely related to Millettieae. These related taxa include representatives from tribes Robinieae (sensu Lavin and Sousa, 1995
), Phaseoleae, Indigofereae, Abreae, Dalbergieae, and species from the temperate herbaceous tribes (Sanderson and Wojciechowski, 1996
). Species from tribe Swartzieae and Sophoreae were used as outgroups based on traditional classification (Polhill, 1981
) and results of rbcL sequence analysis (Doyle et al., 1997
). Samples from Loteae and Coronilleae were selected to complete the sampling for the epulvinate legumes, taxa traditionally associated with the IR-lacking tribes because of a shared loss of the leaf pulvinus. Table 1 lists all the taxa used in this study and the sources, voucher specimen data, and GenBank accession numbers. Samples were collected from either field or herbarium specimens or were extracted freshly from plants germinated from seeds provided by USDA (United States Department of Agriculture) (Table 1). Total genomic DNAs were isolated from fresh or dried materials using standard CTAB extraction methods (Doyle and Doyle, 1987
) or by a protocol designed for rain forest species (Scott and Playford, 1996
), which can remove most of the polysaccharides and secondary metabolites from plant samples. For samples of the tribes Swartzieae, Sophoreae, Dalbergieae, and Aeschynomeneae, DNA isolations, polymerase chain reaction (PCR) amplifications, and fragment purifications were performed with the appropriate QIAGEN kit (QIAGEN Inc., Santa Clarita, California, USA).
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) and reverse (trnK2R) primers were used in amplification reactions, but for some Millettieae members, alternative primer pairs were used to improve the amplification reaction, i.e., trnK1L/matK1932R and trnK685F/trnK2R (see Table 2 for primer design). VentR DNA Polymerase (New England Biolab Inc., Beverly, Massachusetts, USA) was used in most of the reactions due to its high fidelity, but in some recalcitrant samples, Taq polymerase (Promega Corp., Madison, Wisconsin, USA) was used to increase the product yield. Typical conditions for PCR were 4 min at 94°C for initial denaturation, followed by 35 cycles of 30 s at 94°C, 90 s at 48°–50°C for annealing, 2 min and 30 s at 72°C for primer extension, and after the cycles, a final 7-min incubation at 72°C was employed to complete the reaction. PCR products were then analyzed by gel electrophoresis, purified by differential filtration through Ultrafree-MC columns (Millipore, Bedford, Massachusetts, USA).
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Sequence alignment and phylogenetic analyses
Amplified PCR products were ~2.5 kb (trnK1L/trnK2R primer pair) in length. The sequences used for phylogenetic analysis are partial sequences of the trnK intron, which includes the entire matK gene coding region (~1.5 kb) and the 5’ and 3’ end flanking sequences of the trnK intron. The highly variable noncoding regions provided more informative sites for the parsimony analysis.
Sequences were amenable to manual alignment because, in part, of the occurrence of few insertions and deletions (indels) in the matK gene. Manual alignments were evaluated with the program CLUSTAL W (Thompson, Higgins, and Gibson, 1994
). The aligned data matrix and the tree files are available in the EMBL alignment database (Stoesser et al., 1998
) in NEXUS format (Maddison, Swofford, and Maddison, 1997
). Parsimony analysis was performed with PAUP 3.1.1 (Swofford, 1993
) using the heuristic search option with random addition sequences (1000 replicates; see Maddison, 1991
), branch-swapping algorithm set to TBR (tree bisection-reconnection), and the MULPARS and STEEPEST DESCENT options in effect. Gaps were treated as missing data in all analyses. Bootstrap analyses were used to assess the robustness of the trees with 100 replicates for parsimony analysis (Felsenstein, 1985
), and 1000 replicates for neighbor-joining analysis. Neighbor-joining (NJ) analysis was conducted using beta test version 4.0b1 of PAUP* (Swofford, 1999
), and an HKY85 model (Hasegawa, Kishino, and Yano, 1985
) was employed to estimate the distances between sequences. MacClade 3.07 (Maddison and Maddison, 1992
) was used to examine the distribution of molecular and morphological attributes on the cladograms.
RESULTS
Phylogeny based on DNA sequences
We sampled 62 taxa from 57 different genera of Papilionoideae (Table 1). The trnK/matK data matrix provides more resolved phylogenetic relationships for Millettieae than does either rbcL (Doyle et al., 1997
) or the phytochrome gene family (Lavin et al., 1998
). Similar patterns are also found in other groups of plants, where matK sequences tend to have more phylogenetically informative sites than rbcL (Manos and Steele, 1997
).
The 5' and 3' ends of the aligned trnK/matK data matrix close to primer regions were excluded, as were some unalignable parts in the noncoding regions of trnK intron. Of the remaining 2874 included characters, 1585 (55%) were variable, and 1030 (36%) were parsimony informative. Sequence divergence values based on total character difference (raw data) vary from 0.008 substitution per site (between two Wisteria species) to 0.184 substitution per site (between Pisum and Vigna). Within the whole data set, the ratio of terminal taxa (62) to informative characters (1030, excluding informative gaps) was 1:16.6.
Parsimony analysis produced 12 equally most parsimonious trees of 3892 steps with a consistency index (CI) = 0.56 (excluding autapomorphies) and a retention index (RI) = 0.75. Figure 1 shows the strict consensus tree and the internal support from the bootstrap analysis. Figure 2 shows the comparison of the bootstrap trees using parsimony (Fig. 2, left) and the neighbor-joining (Fig. 2, right) methods, and bootstrap support for internal nodes from both methods is indicated. The two methods give very similar topologies, but with slightly different support on the internal nodes. Three taxa also show incongruence on the trees, i.e., Poecilanthe, Harpalyce, and Austrosteenisia (see below for details).
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), where the tribe Desmodieae (not sampled here) is also placed in this major clade. These three taxa together formed a well-supported clade with 95% bootstrap support for parsimony and 97% for NJ analysis (Fig. 2). Within core Millettieae, a "clade A" is recognized, including Tephrosia, Derris, Lonchocarpus, and two sampled Millettia species. Tephrosia and Mundulea are the sister taxa to the rest of the clade A species (Fig. 1) with bootstrap support of 80% (Fig. 2). The sister clade of clade A comprises five taxa: three Philenoptera species (including Capassa), Millettia grandis from Millettia Section Compressogemmatae, and Millettia leptobotrya (=Fordia leptobotrys (Dunn) Schot; see Discussion for details). Our results suggest that the three sampled Philenoptera (including Capassa) species form a clade (100% bootstrap support; Fig. 1), and Millettia grandis and Millettia leptobotrya are the sister groups. Within clade A, Pongamiopsis amygdalina/Millettia thonningii/Neodunnia richardiana formed a distinct group with 96% bootstrap support (parsimony). Three other pairs of taxa also show relatively high bootstrap support, Lonchocarpus lanceolatus/Millettia dura (100%), Paraderris elliptica/Derris laxiflora (100%), and Brachypterum robusta/Fordia splendidissima (94%; bootstrap values refer to parsimony analysis; Fig. 2). The rest of the clade shows less bootstrap support (lower than 80%), and is unresolved.
Two genera, Poecilanthe and Cyclolobium, which have been variously included in Millettieae or other groups, are distantly related to the core Millettieae clade (Fig. 1). Both taxa belong to a clade consisting of taxa from Brongniartieae, and Sophoreae, i.e., Bolusanthus, Ormosia, and Acosmium. Support for the monophyly of Poecilanthe, Cyclolobium, and Brongniartieae is very high (100% from both parsimony and NJ criteria), even though there are differences in the positions of Poecilanthe and Harpalyce in the two methods (Fig. 2).
The topology for the rest of the Papilionoideae is well resolved (Fig. 1). The IRLC, which includes the two Millettieae genera Callerya and Wisteria, is well supported. The sister group of the IRLC is a clade consisting of tribes Robinieae, Loteae, and Coronilleae (sensu Polhill, 1981
). The two clades together, designated as Hologalegina (Fig. 1), is supported by 100% bootstrap support. This Hologalegina clade is not equivalent to the "Hologalegeae" in the previous studies (Lavin et al., 1998
), in which "Hologalegeae" does not include Robinieae, Callerya, and Wisteria.
Psoralea (Psoraleeae) is embedded in the Phaseoleae s.s. (sensu stricto) clade with 100% bootstrap support, in agreement with the rbcL results (Doyle et al., 1997
). Indigofereae is the sister group of the whole Millettieae/Phaseoleae clade (Old World tropical tribes; Fig. 1) with 84% bootstrap support, which is also consistent with the rbcL phylogeny (Doyle et al., 1997
). Sophoreae and Dalbergieae, on the other hand, are para- or polyphyletic at the base of the Papilionoideae (Fig. 1). Part of the Dalbergieae (Dalbergia, Machaerium, and Pterocarpus) are grouped with taxa from Aeschynomeneae (100% bootstrap support; Fig. 1). The support for a group marked by a 50-kb inversion in chloroplast DNA (Doyle et al., 1996
) is high (96% bootstrap support indicated in Fig. 1).
Character evolution in Millettieae and its allies
The distribution of four morphological characters was examined by superimposing characters on the trnK/matK tree as shown in Figs. 3–6
. The distribution of canavanine on the legume phylogeny suggested that the ability to accumulate canavanine has been lost in several lineages. The result shows that canavanine is absent in two Millettieae (Dalbergiella and Ostryocarpus), Phaseoleae s.s., Abreae, and part of core Millettieae. Panicles and pod morphologies are not synapomorphies for Millettieae since none of the characters, alone or in combination, can distinguish a specific clade. However, a pseudoraceme/pseudopanicle clade can be recognized, corresponding to the "core Millettieae"/Phaseoleae clade (Fig. 4).
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Core Millettieae group
Analysis of trnK/matK phylogenies reveals a well-supported clade, as the "core Millettieae" clade (Figs. 1, 2). This clade comprises ~70% of the Millettieae species (sensu Geesink, 1984
) and includes four major genera, Tephrosia, Millettia, Lonchocarpus, and Derris. Our reason for naming this clade is to provide a guideline for a new definition of Millettieae. Core Millettieae, as previously discussed in the context of phytochrome gene phylogeny (Lavin et al., 1998
), consists of two clades, a Tephrosia clade and a Derris-Lonchocarpus clade, but does not include Millettia grandis. We now extend the definition of the core Millettieae to include the Philenoptera clade, which includes Philenoptera (including Capassa), Millettia grandis, and Millettia leptobotrya. The newly defined core Millettieae will now include three major components, the Philenoptera clade, the Tephrosia clade, and the Derris-Lonchocarpus clade.
This circumscription of the core Millettieae suggests that Lonchocarpus and Derris and allies are not closely related to Dalbergieae as suggested by Bentham (1860)
, but rather to Millettia and Tephrosia. This finding does not support the taxonomy of Sousa and de Sousa (1981)
, who considered Lonchocarpus and close relatives to be much more closely related to Dalbergieae. The genera around Lonchocarpus, i.e., Lonchocarpinae sensu Sousa and de Sousa (1981)
, have been placed in Dalbergieae by Bentham (1860
, as subtribe Lonchocarpeae) and Polhill (1971)
, or as a separate tribe Lonchocarpeae, close to Dalbergieae (Hutchinson, 1964
). Lonchocarpinae was thought to be most closely related to Dalbergieae as evinced by its putative cymose inflorescence and indehiscent and winged fruits (Sousa and de Sousa, 1981
). The results from trnK/matK and phytochrome gene family phylogenies do not support this view since no Dalbergieae species are close to the core Millettieae clade. Similarly, Tephrosia and allies are not closely related to Robinieae in the trnK/matK phylogeny, in contrast to the conclusions of Sousa and de Sousa (1981)
.
A well-supported Philenoptera clade, consisting of three species of Philenoptera (including Capassa violacea), Millettia grandis, and Millettia leptobotrya, is the sister group to the rest of the core Millettieae. The segregation of Philenoptera, the so-called African Lonchocarpus (formerly subgenus Paniculati of Lonchocarpus), from the genus Lonchocarpus leaves only one or possibly two (Lock, 1989
) species of this genus in Africa. Other pantropical Lonchocarpus species have been transferred to Disynstemon, Kunstleria, Millettia, or Derris (Polhill, 1971
), but these are yet to be sampled for trnK/matK sequence variation. However, an ongoing survey of Lonchocarpus species based on nuclear ribosomal internal transcribed spacer (ITS) sequences supports the monophyly of New World Lonchocarpus for over 15 taxa from sampled Lonchocarpus so far (Hu et al., unpublished data). The monotypic genus Capassa Klotzsch, which has been discussed in detail by Mendonça and Sousa (1965)
and Polhill (1971)
, was provisionally placed in Philenoptera based on its similarity to Philenoptera laxiflora (Geesink, 1984
). The pod of Capassa violacea has a thin wing along the upper suture, which is considered unusual for Lonchocarpus. The trnK/matK phylogenies support the close relationship between Capassa and Philenoptera with these taxa forming a monophyletic group (Fig. 1).
The circumscription of the genera Derris and Millettia is very complicated, and their classification at the species level has troubled taxonomists. Many specimens have only been identified to genus. Misidentification is very common for these groups if only flowering or fruiting material is available (F. Adema, personal communication, Rijksherbarium, and authors' observations). There are five sections in Derris based on Bentham's (1860)
system. Geesink (1984)
lumped the section Aganope into Ostryocarpus (discussed below) and divided the rest of the genus Derris Lour. into three genera, Derris s.s. (includes Derris sections Euderris and Dipteroderris), Paraderris (formerly Derris section Paraderris), and Brachypterum (formerly Derris section Brachypterum). Here we show that Derris and Paraderris form a monophyletic group, and Brachypterum is the sister group of Fordia (Figs. 1, 2). In contrast, the four Millettia species sampled here are not closely related (Fig. 1). In Dunn's (1912)
classification, Millettia grandis (sect. Compressogemmatae) and Millettia leptobotrya (sect. Albiflorae) are distantly related to Millettia dura and Millettia thonningii (sect. Sericanthae). Millettia grandis and Millettia leptobotrya are distinguished from other Millettia species by a combination of pseudopaniculate inflorescences and the presence of canavanine in seeds (see discussion below). However, the pseudopanicle is not restricted to sections Compressogemmatae and Albiflorae, it can occasionally occur in some other species of Millettia, e.g., M. psilopetula (section Truncaticalyces) (Gillett, 1971
), and M. urophylloides (section Efulgentes) (Dunn, 1912
), and not all species in section Compressogemmatae have pseudopanicles (e.g., Millettia micans has pseudoracemes). In addition, canavanine is present in at least 15 other Millettia species (excluding the species transferred to Callerya) (Evans, Fellows, and Bell, 1985
). Until more intensive sampling is undertaken, any conclusion as to the classification of Millettia would be premature.
Geesink (1984)
raised Millettia section Albiflorae (including Millettia leptobotrya) to a new genus, Imbralyx, but no nomenclatural combination was made for the taxa other than the type species. Imbralyx was treated under Fordia based on cladistic analysis of morphological and anatomical characters using Millettia pulchra as the outgroup (Dasuki and Schot, 1991
; Schot, 1991
). However, the rooting position of the tree is problematic. The analysis did not include other outgroup taxa to eliminate the possibility that the tree does in fact have Imbralyx as the outgroup taxon, and Fordia species and Millettia pulchra forming a clade. If this is the case, then Imbralyx should not be judged as part of Fordia (Dasuki and Schot, 1991
; Schot, 1991
), therefore the name of Imbralyx should remain at this point. The trnK/matK phylogenies show strong support for distinguishing Millettia leptobotrya and Fordia splendidissima (Figs. 1, 2), and thus we leave the name of Millettia leptobotrya unchanged. Re-establishing the genus Imbralyx seems reasonable.
Fordia and Brachypterum, which are sister groups with fairly high support (94% from parsimony, 81% from NJ; Fig. 2), share few morphological similarities, and, again, this raises more questions about relationship in the Millettia/Derris complex, where support among groups is low and more sampling of taxa and characters is necessary.
Genera Abrus, Galactia, and Ophrestia
Abrus, a small pantropical genus with 17 species, is usually placed in its own tribe, Abreae (Polhill, 1981
). The relationship of Abreae to other tribes based on morphology is problematical. It has affinities with the Vicieae because of its twining stems and paripinnate leaves ending in a bristle (Hutchinson, 1964
), with Dalbergieae and Phaseoleae because of its general appearance (Baillon, 1870), and with African Millettia because of its tendency to twine, its pseudoracemes, and a similar geographical distribution (Polhill, 1981
). Our tree confirms that Abrus is the sister group to the core Millettieae plus Galactia, a similar result to that found with rbcL data (Doyle et al., 1997
), but it is not close to the temperate herbaceous clade as suggested in another rbcL study (Käss and Wink, 1997
). This supports the idea that the Abrus precatorius sampled in the paper of Käss and Wink (1997)
was misidentified (Doyle et al., 1997
). Furthermore, Abrus shares with core Millettieae members a pseudoraceme inflorescence, an absence of canavanine (except in the Philenoptera clade), and chromosome number of x = 11.
In the rbcL studies (Doyle et al., 1997
), Canavalia (subtribe Diocleinae of Phaseoleae) was shown to be the sister group to Tephrosia and Derris. Here another genus of Diocleinae, Galactia, appear to be sister to the core Millettieae clade (Figs. 1, 2). This result is congruent with chloroplast DNA restriction site analysis (Bruneau, Doyle, and Doyle, 1994
) with Diocleinae being the sister group of the samples of Millettieae in that study. However, the trnK/matK phylogeny places Ophrestia within Phaseoleae s.s. (Fig. 1), whereas it is the sister group of the Millettieae/Phaseoleae clade in the chloroplast DNA restriction site analysis (Bruneau, Doyle, and Doyle, 1994
).
Genera of Millettieae not in the core Millettieae clade
Six taxa, Platycyamus, Dalbergiella, Ostryocarpus, Austrosteenisia, Cyclolobium, and Poecilanthe, are excluded from the core Millettieae clade. Platycyamus, which was placed in Phaseoleae in Hutchinson's (1964)
system and by studies based on floral and leaf characters (Lackey, 1978, 1979
), is the sister group of Phaseoleae s.s. (excluding Diocleinae), based on trnK/matK results (Figs. 1, 2). Sousa and de Sousa (1981)
treated Platycyamus under Dalbergieae because of its flowers with a well-developed hypanthium and a winged and indehiscent pod. However, Geesink (1984)
transferred Platycyamus to Millettieae because of its similarity to Derris and Craspedolobium and the presence of canavanine in its seeds. Our results show that Platycyamus is more closely related to Phaseoleae, which suggests that the enlarged basiscopic side of the lateral leaflets is a synapomorphy for the Platycyamus plus Phaseoleae clade.
Dalbergiella was first included in Millettieae by Geesink (1981)
, but he later excluded it and aligned it with Dalbergieae (Geesink, 1984
) because of its free vexillary stamen, wings free from keels, and absence of nonprotein amino acids. However, the non-protein amino acids are also absent in Austrosteenisia and Ostryocarpus (Evans, Fellows, and Bell, 1985
). In fact, trnK/matK data suggest that there might be several parallel gains and losses for nonprotein amino acids in Papilionoideae (Fig. 3). In addition, Dalbergiella is atypical of the genera of Dalbergieae in having the free part of the stamens less than half as long as the fused part. Therefore, the morphological evidence for keeping Dalbergiella in Dalbergieae is weak. Phylogenies derived from trnK/matK sequences reveal that Dalbergiella nyasae is not close to Dalbergieae (represented here by Dalbergia, Vataireopsis, Andira, Pterocarpus, and Machaerium) (Fig. 1), but instead is much closer to the core Millettieae.
Geesink (1984)
combined Ostryoderris, Xeroderris, and Derris section Aganope into Ostryocarpus, mainly due to their truly paniculate inflorescences, free wing petals, and indehiscent pods. Geesink (1984)
also stated that Ostryocarpus and Callerya are nearly indistinguishable, especially in their paniculate inflorescences and flowers with free wing petals, and free vexillary stamen. Geesink (1984
, p. 109) also noted that they both lack canavanine and other nonprotein amino acids or amines, but he may have been mistaken, since according to the reference cited (Evans, Fellows, and Bell, 1985
), Callerya does, in fact, accumulate canavanine. Nevertheless, it was correctly scored in his phylogenetic data matrix (Geesink, 1984
, table 6.3). Ostryocarpus, however, lacks nonprotein amino acids as do other Millettieae basal to the core group (except Platycyamus). Ostryocarpus stuhlmannii [= Xeroderris stuhlmannii (Taub.) Mendonça & Sousa], from semi-arid tropical Africa, is not sister to Pongamiopsis as indicated by the phytochrome tree (Lavin et al., 1998
), but in any case it is not closely related to Callerya as suggested by Geesink (1984)
.
The trnK/matK phylogeny places Austrosteenisia blackii in an isolated position from core Millettieae (Fig. 1), but has a higher support as the sister group of the core Millettieae/Phaseoleae clade in NJ analysis (Fig. 2). It is clear that this species is distinct from Millettia and Lonchocarpus, in which it was formerly placed. We did not include Kunstleria, a genus closely related to Austrosteenisia (Dixon, 1997
), in our analyses. Kunstleria, despite its similar appearance and geographical distribution to Austrosteenisia, has the vexillary stamen free but connate to the claw of the standard (Ridder-Numan and Kornet, 1994
; Ridder-Numan, 1995
). It remains to be determined whether Kunstleria also belongs to the core Millettieae.
Cyclolobium and Poecilanthe have been moved in and out of Millettieae in the literature (Polhill, 1981
; Geesink, 1984
; Lavin and Sousa, 1995
). Cyclolobium is similar in vegetative morphology to Ostryocarpus, but differs in its one-foliolate leaves (Geesink, 1984
). The chromosome number of Cyclolobium, x = 9, is unusual in Millettieae but is common in some genera of Sophoreae, such as Bolusanthus, Calpurnia, and Acosmium, as well as in Brongniartia (Brongniartieae) (Goldblatt, 1981
). Poecilanthe has been placed in Dalbergieae (Bentham, 1860
; Lavin, 1987
), Millettieae (Hutchinson, 1964
; Lavin and Sousa, 1995
), or Robinieae (Geesink, 1984
). It has been suggested as a relative of Brongniartieae based on anther and pod morphology (Lavin, 1987
), and alkaloid profiles (Greinwald et al., 1995
). The trnK/matK phylogenies strongly support a close relationship between these two taxa and Brongniartieae (Figs. 1, 2), placing them in a small clade containing taxa from Sophoreae (Acosmium, Bolusanthus, and Ormosia) (Figs. 1, 2). The chromosome number of Poecilanthe has not been determined, and Poecilanthe and Cyclolobium share very few features except for one-foliolate leaves that are occasionally found in Poecilanthe. Further detailed study is needed.
Callerya and Wisteria
The evidence that these two genera are very distinct from other Millettieae species continues to mount, as suggested by surveys of the chloroplast inverted repeat (Lavin, Doyle, and Palmer, 1990
; Liston, 1995
), rbcL (Doyle et al., 1997
), phytochrome gene family (Lavin et al., 1998
), and ndhF (Diederick et al., unpublished data). Moreover, both Callerya and Wisteria have a basic chromosome number, x = 8, which is the same as most of the temperate herbaceous tribes in Papilionoideae (Goldblatt, 1981
; Hu, unpublished data). In comparison, either x = 11 or 12 is common within Millettieae (Goldblatt, 1981
), though x = 10 in Leptoderris and Aganope (= Ostryocarpus), and x = 8, 10, 11, 12, 18 in Millettia. Millettia drastica Welw. ex Baker, a tropical African tree, is the only Millettia that has a chromosome number x = 8 (Gill and Husaini, 1982
). Whether or not it is close to Callerya remains to be evaluated with molecular sequence data.
Wisteria (including Millettia japonica) is one of the few exceptional Millettieae distributed in temperate regions, and thus it might not be surprising that molecular evidence reveals its close relationship to other temperate groups. However, Callerya has a subtropical/tropical distribution as well as woody habit, which does not match most taxa in the IR-lacking clade.
Notably, the genus Callerya, comprising Millettia section Eurybotrya and two distinct genera Padbruggea and Whitfordiodendron, can only be distinguished from Millettia by seemingly trivial characters, such as paniculate inflorescences and diadelphous stamens (Schot, 1994
). Worse yet, precisely these same two features are variably present in several other genera of the Millettieae group, and Callerya is thus indistinguishable from them. For example, panicles occur in about half the genera in Millettieae (Geesink, 1984
). Eight of these (Behaimia, Craibia, Dewevrea, Endosamara, Kunstleria, Ostryocarpus, Platycyamus, and Sarcodum) also possess diadelphous stamens and can only be distinguished from Callerya by combinations of character states, such as alternate leaflets and a cupular aril in Craibia, or a lomented endocarp in Endosamara. trnK/matK phylogenies show that Ostryocarpus and Platycyamus do not belong to the Callerya group, nor the core Millettieae clade. There is no molecular evidence for several other paniculate genera, and it will be interesting to see where these taxa fit into the phylogeny when they are sequenced.
The monophyly of the IR-lacking group is well supported in our trnK/matK phylogeny (100% bootstrap value; Figs. 1, 2), and the loss of IR is indeed a distinct feature in Papilionoideae phylogeny. Callerya, Wisteria, and Glycyrrhiza (tribe Galegeae) are the sister groups to the rest of the IR-lacking clade (IRLC) (Fig. 1). However, the relationships between these three genera and the rest of the IRLC remain unresolved (Fig. 1). The phylogeny derived by NJ analysis shows weak support for the Callerya/Wisteria clade (Fig. 2), but this is less resolved in the parsimony analysis (Fig. 2). Callerya atropurpurea causes the ambiguity in the phylogeny of IRLC, since the phylogeny is more resolved when it is removed from the data matrix (Hu, unpublished data).
Character evolution in Millettieae and its allies
The nonprotein amino acid canavanine has been used as a character in the chemotaxonomy of legumes (Bell, Lackey, and Polhill, 1978
; Evans, Fellows, and Bell, 1985
; Polhill, 1994
), although a complete chemical profile is always needed to imply phylogenetic relationships. Here we show that parallel losses of canavanine are common in Papilionoideae, as inferred from the trnK/matK phylogeny (Fig. 3). The character state is equivocal at the base of the Indigofereae-Millettieae-Phaseoleae clade (Fig. 3), but it is clear that the absence of canavanine is more common in the core Millettieae clade. Canavanine is present in Galactia, the Philenoptera clade (all five species), and Platycyamus, but not in Dalbergiella, Ostryocarpus, Austrosteenisia, and most of the core Millettieae species. However, some dispute regarding the presence/absence of canavanine can be found in the literature, either because some taxa sampled for the compound were misidentified, or because there is variation within populations (Rao, 1983
). For example, Evans, Fellows, and Bell (1985)
showed canavanine to be absent in Millettia grandis, but it is present in the survey by Bell, Lackey, and Polhill (1978)
. Similar results were found in Millettia thonningii, where Evans, Fellows, and Bell (1985)
showed no canavanine in this species, but Bell, Lackey, and Polhill (1978)
did. Canavanine is reported in Tephrosia grandiflora and Tephrosia incana (Bell, Lackey, and Polhill, 1978
), but Evans, Fellows, and Bell (1985)
showed the lack of canavanine for these two species. Again in Mundulea sericea, canavanine was absent according to Bell, Lackey, and Polhill (1978)
and Evans, Fellows, and Bell (1985)
, but present according to Rao (1983)
. Therefore, we consider these species can, or at least have the potential to produce canavanine. The rest of core Millettieae species accumulate other nonprotein amino acids (e.g., modified homoarginine) instead of canavanine, suggesting that the function of canavanine can be replaced (Evans, Fellows, and Bell, 1985
). It is possible that Millettia thonningii, Tephrosia grandiflora, Tephrosia incana, and Mundulea sericea are in a transitional state of using either canavanine or other nonprotein amino acids for chemical defenses or storage, functions suggested by Rosenthal (1990)
. It seems possible that the accumulation of nonprotein amino acids in seeds evolved from the most recent common ancestor of Hologalegina and Indigofereae-Millettieae-Phaseoleae clade, with very few cases of loss or reversal to alkaloid accumulation (i.e., Abreae), as shown on Fig. 3.
Of the other three morphological characters shown on Figs. 4–6, the inflorescence type, winged pod, and dehiscent pod, none unambiguously corresponds to a monophyletic group. A paniculate inflorescence has been suggested to be the primitive type of inflorescence in the Dalbergieae-Millettieae group (Geesink, 1984
), but this is not supported by the phylogenetic distribution shown in Fig. 4. The presence of panicles in Callerya is unusual in the IRLC or the Robinieae-Loteae-Coronilleae clade. It is possible that the panicle of Callerya is derived from a pseudoraceme or pseudopanicle inflorescence type by elongation of the secondary axes, as proposed by Geesink (1984)
. However, the recognition of a pseudoraceme/pseudopanicle group (marked by an arrow on Fig. 4) is of interest, but other paniculate Millettieae taxa should be sampled for further morphological phylogenetic analysis.
Lastly, we find very high support for the core Millettieae clade, which includes all of the fruit types that have been used to distinguish higher taxa (e.g., tribes and subtribes) by Bentham and others. Since these character states occur repeatedly both inside and outside core Millettieae, there is strong support for high levels of homoplasy. This suggests that fruit characters should carry little weight in the classification of Millettieae. For example, winged pods, which might be a general adaptation for wind dispersal, have evolved at least several times in legumes (e.g., Fig. 5). Also, dehiscent pods are difficult to define because the tardy condition can be found in indehiscent pods, as in the fruits of Pongamia pinnata, and it is apparent that the dehiscence of pods also has evolved several times in legumes (Fig. 6). Conversely, despite the great similarities of the fruits of "Lonchocarpinae" (Lonchocarpus, Derris, and their allies) and Dalbergieae, these taxa are not closely related. As Polhill, Raven, and Stirton (1981
, p.17) stated (in legume taxonomy), "it is probably fair to say that more errors in generic and tribal concepts have been made from overweighting obvious fruit characters than from any other consideration."
FOOTNOTES
1 The authors thank Frits Adema, Yu-Chung Chiang, Haroldo C. de Lima, Colin Hughes, Matthew Johnson, Aaron Liston, Toby Pennington, Kuo-Chen Yang, and the staffs of U. S. Department of Agriculture for providing plant materials and seeds; and Hang Sun, Xiue-Dung Li, and Baogui Li for help with field collections in China and permission for examination of herbarium specimens. This work was supported by grants from the Center for Biosystematics, University of California, Davis, and a Stebbins Grant from the Davis Herbaria Society to JMH, and National Science Foundation (DEB 95–96279) to MJS and MFW. 
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