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Systematics |
2School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand; 3Department of Botany, University of Texas at Austin, Austin, Texas 78712 USA
Received for publication October 2, 2001. Accepted for publication March 21, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Alsinoideae • Caryophyllaceae • Caryophylloideae • ndhF • Paronychioideae • phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Despite continuing research into aspects of the biology of its members, the generic and higher level systematics of the Caryophyllaceae has been largely neglected until recently. This neglect may be partly due to the high level of morphological homoplasy that obscures relationships between genera and species, the attention focused on questions of interfamily relationships in the order Caryophyllales (R. Rabeler, University of Michigan, personal communication), and perhaps partly to the existence of many poorly known genera.
Although the family Caryophyllaceae as a whole is well defined by apomorphic characters, at this time subfamilial taxonomy in the Caryophyllaceae is not firmly based on a knowledge of phylogeny (Bittrich, 1993
). However, a number of subfamilies and tribes are widely recognized (Rabeler and Bittrich, 1993
). Three subfamilies (Paronychioideae, Alsinoideae, and Caryophylloideae) have been widely accepted within the Caryophyllaceae, but the delimitation of each has varied between authors. Only subfamily Caryophylloideae is well supported by morphological apomorphies (possession of a calyx tube, corolla scales, closed petal venation, and seed morphology). Within the Caryophylloideae, molecular-phylogenetic studies of the tribe Sileneae (Oxelman and Liden, 1995
; Oxelman, Liden, and Berglund, 1997
; Oxelman, et al., 2001
) have revealed the inadequacy of the current classification and the difficulty in distinguishing strictly monophyletic genera.
Bittrich (1993)
tentatively argued that most genera of the subfamily Alsinoideae possess nectary glands on the base of their stamens and that this may be a synapomorphy for the subfamily. Otherwise, the Alsinoideae are a diverse group and are possibly paraphyletic (Bittrich, 1993
). The remaining subfamily, Paronychioideae, is particularly poorly defined. Bittrich (1993)
circumscribed Paronychioideae to include all the genera in the family with stipulate leaves. Historically some weight has also been attached to fruit characters. In particular, the indehiscent fruits of many Paronychioideae are contrasted with the capsules of most Alsinoideae and Caryophylloideae. However, several genera usually included in the Alsinoideae have indehiscent fruits (e.g., Scleranthus, Habrosia, and Plettkea: Bittrich, 1993
) and capsules characterize the Paronychioideae tribe Polycarpeae. Subfamily Paronychioideae, or a part of it, has sometimes also been recognized as a distinct family, the Illecebraceae (e.g., Hutchinson, 1974
), but this segregation has not been recently defended.
In addition to these problems of circumscription, relationships among the three subfamilies are unclear. Bittrich (1993)
suggested subfamilies Alsinoideae and Caryophylloideae form a monophyletic group. Further, he suggests that chromosome numbers and the type of embryogeny (Solanad, in at least some Paronychioideae; generally Caryophyllad in Alsinoideae and Caryophylloideae) are important characters supporting the monophyly of Caryophylloideae and Alsinoideae together. However, embryogeny has not been widely surveyed in Paronychioideae and the Caryophyllad type may be ancestral in the family as whole. Bittrich also suggested that Caryophylloideae themselves are derived from "advanced" Alsinoideae (on the basis of chromosome numbers), thus making Alsinoideae paraphyletic. Within the three subfamilies, genera have been assigned to several tribes. As the most recent, Bittrich's classification scheme is shown in Table 1.
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During the 1990s there was extensive application of molecular phylogenetics to questions of angiosperm origin and to relationships and monophyly of major and intractible plant families. A common result was the discovery that long established pairs of related families often included one monophyletic family nested within a paraphyletic one (e.g., Ericaceae; Kron, 1996
). Generic studies have also shown similar patterns (e.g., Hebe/Parahebe/Veronica: Wagstaff and Garnock-Jones, 1998
; Lycopersicon/Solanum: Spooner, Anderson, and Jansen, 1993
). A few infrafamilial studies (e.g., Asteraceae: Kim and Jansen, 1995
; Labiatae: Wagstaff et al., 1998
) have demonstrated the paraphyly or polyphyly of long-established subfamilies and tribes. Such studies are important for the organization and interpretation of knowledge about biodiversity, the testing of evolutionary and biogeographic hypotheses, and the establishment of appropriate outgroups for studies within genera.
Ideally, DNA sequence studies can provide completely resolved phylogenies, but in a large group this requires extensive taxon sampling. Also, in many cases, phylogenies based on single gene sequences are likely to be misleading because characters are not inherited independently or are unresolved due to insufficient numbers of characters. Overcoming this can require sequencing DNA from several appropriately evolving regions. Therefore, this study's more limited aims were to identify major monophyletic groups within the Caryophyllaceae, test the monophyly of currently recognized groups, and underscore the need for caution in interpretation and application of nonphylogenetic classifications.
Several genera of Caryophyllaceae with uncertain affinities have been included in the present study in order to test their placement in the Alsinoideae or the Paronychioideae and to test the value of key morphological characters in estimating phylogeny in this family. Evaluation of morphological characters of Scleranthus has been insufficient to determine its affinities within Caryophyllaceae (Smissen, 1999
). Its very small, apetalous flowers and especially one-seeded indehiscent fruits are the main characters linking it to the Paronychioideae, while its connate leaves and lack of stipules link it to the Alsinoideae. Conversely, stipulate leaves link Spergularia to the Paronychioideae (Bittrich, 1993
), while its capsules and free styles link it to the Alsinoideae. Drymaria is another genus included in the Paronychioideae, with reservations, by Bittrich (1993)
. According to him, its stipules develop differently from those of other Paronychioideae and it shows some characters more typical of the Alsinoideae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Weak support for this relationship was also obtained from analysis of restriction fragment variations (Downie and Palmer, 1994
). However, a clade comprising the families Chenopodiaceae and Amaranthaceae appeared as sister group to Caryophyllaceae in analyses of rbcL (Manhart and Rettig, 1994
) and ORF2280 (Downie, Katz-Downie and Cho, 1997
) DNA sequences.
DNA was extracted from fresh leaves by the cetyltrimethylammonium bromide(CTAB) method (Doyle and Doyle, 1987
) and purified by phenol chloroform extraction (Sambrook, Fritsch, and Maniatis, 1989
). Then 1-µL aliquots of DNA extracts or a 1/10 dilution thereof were used in subsequent polymerase chain reaction (PCR). To amplify the 5' region of ndhF, versions of primers ndhF15 and ndhF8 with a number of degenerate sites were used (see below for primer sequences). In addition to DNA template, PCR reactions contained 1 unit of Taq DNA Polymerase (Amersham Pharmacia Biotech, Piscataway, New Jersey, USA), 2.5 µL 10x reaction buffer (500 mmol/L KCl, 15 mmol/L MgCl2, 100 µmol/L Tris-HCl pH 9.0), 10 pmol each primer, 42.5 µmol/L MgCl2, 25 ng BSA and H2O to make up a total volume of 25 µL. Cycling conditions were 96°C for 30 s, 50°C for 45 s, 70°C for 2 min, for a total of 30 cycles. The PCR products were electrophoresed on 1% agarose using TBE buffer (Sambrook, Fritsch, and Maniatis, 1989
) to check their size, quality, and quantity.
Three sequencing methods were used to generate the data used in this study as alternative technologies became available in our laboratory.
Firstly, double-stranded DNA (dsDNA) PCR products were purified by agarose gel electrophoresis and a second round of PCR using either ndhF15 or ndhF8, and one of the internal primers ndhF536 or ndhF972R at stringent annealing temperatures (65°C) was used to produce dsDNA template for cycle sequencing. Products were again purified by agarose gel electrophoresis and DNA recovered from the agarose gel using Prep-a-gene kits (Biorad, Hercules, California, USA; catalogue number 732-6016) according to the manufacturer's guide. Between 3 and 6 µL of DNA template was used in cycle sequencing reactions with the ABI Prism Dye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, Foster City, California, USA; P/N 402078), 3.2 pmol sequencing primer, and H2O to make up a final volume of 20 µL. The labeled products were analyzed by electrophoresis on an ABI Prism 377 DNA sequencer.
Secondly, PCR products were purified by electrophoresis as above and a second round of PCR carried out using modified ndhF8 or ndhF15 primers tailed with the M13 forward universal sequencing primer sequence and one of the internal primers ndhF536 or ndhF972R annealing at 65°C. Products were again purified by agarose gel electrophoresis and Biorad Prep-a-gene system and recovered DNA used as template in cycle sequencing reactions with Applied Biosystems ABI Prism Big Dye Dye Terminator Cycle Sequencing Ready Reaction Kit (P/N 4303149) and 3.2 pmol M13-21 primer or Applied Biosystems ABI Prism M13-21 Big Dye Dye Primer Cycle Sequencing Ready Reaction Kit (P/N402136). Again extension products were separated and detected with an ABI Prism 377 DNA sequencer.
Thirdly, for some sequences, ndhF DNA was PCR amplified and gel purified as above and dsDNA product used as template for PCR with 5' biotinylated versions of either the ndhF8 or ndhF15 primer and one of the internal primers ndhF536 or ndhF972R. Single-stranded DNA was recovered with Dynal m-280 Streptavidin Dynabeads (Dynal Biotech, Smestad, Norway) as described in the manufacturer's instructions. Single-stranded DNA from both biotinylated and unbiotinylated strands were used in sequencing reactions using 35S-labeled deoxyadenesine triphosphate (dATP) in conjunction with Sequenase version 2.0 DNA sequencing kit (US Biochemicals, Cleveland, Ohio, USA; P/N 70770) according to the manufacturers instructions. Primers ndhF15, ndhF536, ndhF536R, ndhF972, ndhF972R, and ndhF8 were used as sequencing primers. Labeled products were separated by electrophoresis.
Sequences obtained from these three methods were combined. Uncertain or ambiguous sites were coded as unknown.
In this study we used modified versions of the previously published primers, ndhF8 and ndhF15 (Olmstead and Sweere, 1994
), to amplify the 5' region of ndhF by PCR as well as novel primers, ndhF476R, ndhF536, ndhF536R, ndhF972, ndhF972R, which were used in sequencing protocols. Primer sequences as used in this study are as follows; ndhF8 ATA GAT CCG ACA CAT ATA AAA TSC RGT T, ndhF15 ATG GAA CAG ACA TAT CAA TAY GSR TG, ndhF476R TTG TTG ACA AGC ACT CGC AGC A, ndhF536 CTC TCA ATT CGG YTA TAT KAT G, ndhF536R TCC CCT ACA CGA TTS GTY ACA A, ndhF972 CTC TCA ATT GGG YTA TAT KAT G, ndhF972R CAT CAT ATA ACC CAA TTG AGA C. The position of sequencing primers and regions of sequence combined for analysis in this study are shown in Fig. 1.
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). All shortest parsimony trees were found using branch and bound searches with MULPARS and steepest descent options in effect. Neighbor-joining trees were constructed from Jukes-Cantor distances with missing data excluded only in those pairwise comparisons affected. Nucleotide frequencies and transition/transversion ratios were estimated by PAUP* 4.0b2 from a selected shortest parsimony tree by maximum-likelihood method using the Jukes-Cantor model of nucleotide substitution with all sites assumed to evolve at equal rate. Pairwise divergences were determined by PAUP* 4.0b2. Numbers of substitutions by codon position were determined by MacClade (Maddison and Maddison, 1992
) from a selected shortest parsimony tree. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A branch and bound search by PAUP*4.0b2 found 12 shortest trees 733 steps long for the aligned 5' ndhF data set. One of these is shown as Fig. 2. A decay analysis was conducted by successively searching for longer trees up to six steps longer than the shortest trees. The decay value indicates the number of additional steps required to collapse a branch. Some clades were found in all trees six steps or less longer than the shortest trees. These are shown in Fig. 2 as having a decay value of >6. The 733 nucleotide changes implied by this tree are distributed among codon positions in the ratio 1.6 : 1 : 5.1 with transitions outnumbering transversions by 1.17 : 1. The tree shown has a consistency index of 0.496, retention index 0.543, and rescaled consistency index of 0.298 (excluding uninformative characters).
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to either tribe Polycarpeae (Polycarpon tetraphyllum, Loeflingia squarrosa, and Drymaria laxiflora) or tribe Paronychieae (Dicheranthus plocamoides and Scopulophila rixfordii). Clade II contains two more species of subfamily Paronychioideae, Herniaria glabra and Paronychia drummondii. Both these species are part of the tribe Paronychieae sensu Bittrich (1993)
. Clade III contains all the representatives of subfamilies Caryophylloideae and Alsinoideae sampled along with Spergularia marina (Polycarpeae sensu Bittrich, 1993
).
A notable feature of this tree is the lack of support for monophyly of any of the tribes of Bittrich (1993)
for which we have sampled more than one species. Species of Polycarpeae are distributed over Clade I (Polycarpon tetraphyllum, Drymaria laxiflora, and Loeflingia squarrosa) and Clade III (Spergularia marina). Moreover, two species of Paronychieae (Dicheranthus plocamoides and Scopulophila rixfordii) group amongst the Polycarpeae included in Clade I. No support is provided for the monophyly of subfamilies Caryophylloideae or Alsinoideae or tribe Alsineae (to which Arenaria, Cerastium, Stellaria and Colobanthus are assigned by Bittrich, 1993
). However contradictory groupings were not supported (or supported very weakly) by the bootstrap analysis. In this analysis, Spergularia marina and Scleranthus biflorus group strongly with the Alsinoideae/Caryophylloideae and not with the exclusively Paronychioideae clades. However, Drymaria laxiflora is well supported as belonging to Clade I along with most of the other Polycarpeae sampled.
The topology of the neighbor-joining tree (Fig. 3) is identical to that of the shortest parsimony tree shown, except that it groups Spergularia marina with Scleranthus biflorus and Silene antirhina. However, internal branch lengths within the Alsinoideae/Caryophylloideae clade are generally very short except for the branch leading to Cerastium glomeratum and Stellaria media.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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are distributed over three clades in both the neighbor-joining and all of the shortest parsimony trees. Support for inclusion of Spergularia marina (tribe Polycarpeae) in clade III along with all the representatives of Alsinoideae and Caryophylloideae is very strong (bootstrap percentages of 100 and 99 in parsimony and neighbor-joining trees, respectively). Bittrich (1993)
noted that Spergula, Spergularia, and Sanctambrosia are the only genera with free rather than connate styles that he included in the tribe Polycarpeae. Most members of the other tribes of Paronychioideae have connate or fused styles. Only two genera included in subfamiliy Alsinoideae by Bittrich (1993)
have connate styles; the remainder have free styles. Further, placement of these two genera, Pycnophyllum and Pentastemonodiscus, in the Alsinoideae is called into question by nrDNA sequences (Smissen, 1999
). All genera of Caryophylloideae have free styles. Styles are fused in Amaranthaceae (Townsend, 1993
) and Chenopodiaceae (Kühn et al., 1993
) but generally free in Molluginaceae (Endress and Bittrich, 1993
), making it unclear what the ancestral condition in Caryophyllaceae is. Further study is required to establish the significance of free or fused styles in Caryophyllaceae, especially which is the apomorphic condition, but transfer of Spergula and Sanctambrosia, along with Spergularia, to Alsinoideae should be considered. It should also be noted that Spergularia and Spergula are probably closely related (Bittrich, 1993
) and have been previously united (Pedersen, 1984
).
Monophyly of the remainder of the subfamily Paronychioideae is neither supported nor contradicted by this study. Paronychioideae (excluding Spergularia) appear as a monophyletic group in the neighbor-joining tree and some, but not all, shortest parsimony trees. This subfamily is not well defined by morphological characters likely to be apomorphic (based on comparison with potential outgroups) and may be paraphyletic. Representatives of tribe Paronychieae (sensu Bittrich, 1993
) are distributed over Clades I and II. This tribe is apparently a polyphyletic grouping of taxa, which have evolved indehiscent fruits with reduced ovule number in parallel. Additional sampling from subfamily Paronychioideae is needed to establish the affinities of individual genera. A likely outcome is that a reduced tribe Paronychieae based on Clade II and an enlarged tribe Polycarpeae based on Clade I can be defined, possibly at subfamily level.
Clade III (comprising the subfamilies Caryophylloideae and Alsinoideae provided Spergularia and Scleranthus are included in Alsinoideae) is well supported by bootstrap and decay analysis. However, none of the analyses was able to resolve relationships among genera within this clade reliably, with the exception of the close sister-group relationship of Stellaria and Cerastium (Figs. 2 and 3).
The two species of Caryophylloideae sampled here, Dianthus caryophyllus and Silene antirrhina, do not appear as a monophyletic group in any of the shortest parsimony trees found by PAUP*4.0b2 or in the neighbor-joining tree. Instead, Dianthus caryophyllus groups weakly with Colobanthus brevisepalus, and Silene antirrhina groups weakly with Scleranthus biflorus and Spergularia marina. However this topology (which implies a multiple origin of the Caryophylloideae from the Alsinoideae) is only very weakly supported by the data. Further, it is hard to reconcile with the morphology of the plants, where Caryophylloideae exhibit several distinct synapomorphies (Bittrich, 1993
), and it is unlikely to be a true reflection of their relationships.
It has previously been suggested that the subfamily Alsinoideae may be paraphyletic because there is a lack of apomorphic characters uniting its members (Bittrich, 1993
). This is consistent with the analyses reported here. The most parsimonious tree in which the Alsinoideae appear as a monophyletic group is six steps longer than the most parsimonious tree found for the data (five steps if Spergularia marina is allowed to be part of this clade). All shorter trees have the Caryophylloideae (represented by Dianthus caryophyllus and Silene antirrhina) nested somewhere within the Alsinoideae although not necessarily together. Very long DNA sequences are likely to be required to fully resolve this part of the Caryophyllaceae phylogeny. A data set produced by combining rbcL and 5' ndhF sequences was unable to resolve relationships among the four species Polycarpon tetraphyllum (Paronychioideae), Stellaria media (Alsinoideae), Dianthus caryophyllus (Caryophylloideae), and Silene antirrhina (Caryophylloideae) despite including 255 variable characters amongst the genera (R. D. Smissen, unpublished data). It is possible that additional data from the more rapidly evolving 3' end of the ndhF gene or from matK might provide better resolution and make wider taxon sampling in this group useful. The greater frequency of substitutions in these faster-evolving sequences makes it more likely that lineages sharing short periods of common descent will have acquired shared substitutions during that time. However, this phylogenetic signal may be obscured by additional phylogenetic "noise" caused by homoplasious substitutions acquired independently in lineages after their divergence. Careful examination of morphological characters and a cladistic treatment of these might provide more insight than DNA sequencing within current practical limitations.
Although 5' ndhF does not fully resolve relationships within the subfamilies of Caryophyllaceae, it has self-evident utility in assessing the affinities of problematic genera. This study confirms that Scleranthus and Spergularia are more closely related to the Alsinoideae than to the Paronychioideae and that Drymaria is a member of one of the two Paronychioideae clades identified. It has also provided compelling support for a clade composed of subfamilies Alsinoideae and Caryophylloideae and confirms the non-monophyly of the tribes Polycarpeae and Paronychieae (subfamily Paronychioideae) as circumscribed by Bittrich (1993)
. A number of other genera could be usefully sampled in a larger data set. Obtaining 5' ndhF sequences for the two genera of the third tribe of the subfamily Paronychioideae, the Corrigioleae (Corrigiola and Telephium) would clearly be desirable, especially as these have also been placed in Molluginaceae (Gilbert, 1987
; but see Downie, Katz-Downie, and Cho, 1997
). Inclusion of sequences from these two genera might also improve resolution of relationships between the three main clades of Caryophyllaceae reported here.
In conclusion, it is clear that chloroplast gene sequences, including ndhF, have much to offer for phylogenetic study of the Caryophyllaceae. A larger study, with longer or more rapidly evolving sequences of DNA and wider taxon sampling, could lay the framework for a stable subfamilial classification. This would facilitate more finely focused evolutionary studies of individual genera or groups of closely related genera such as Scleranthus and the Hawaiian Alsinoideae Schiedea and Alsinidendron (W. Wagner, Smithsonian Institution, personal communication).
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FOOTNOTES |
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4 Author for correspondence (smissenr{at}landcare.cri.nz
)
5 Current address: Landcare Research, PO Box 69, Lincoln 8152, New Zealand
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LITERATURE CITED |
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