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Systematics |
2Molecular Systematics Section, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK; 3National Herbarium of the Netherlands, Utrecht University Branch, Heidelberglaan 2, 3584 CS, Utrecht, The Netherlands; and 4Biological Interaction Section, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK
Received for publication February 22, 2001. Accepted for publication July 27, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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930 base pairs of the matK plastid gene have been sequenced and analyzed for 127 taxa. In addition, these sequences have been combined with the rbcL plastid gene for 53 taxa and with the rbcL and atpB plastid genes as well as the nuclear 18S rDNA for 26 taxa to provide increased support for deeper branches. The red pigments of Corbichonia, Lophiocarpus, and Sarcobatus have been tested and shown to belong to the betacyanin class of compounds. Most taxa of the order are clearly grouped into two main clades (i.e., "core" and "noncore" Caryophyllales) which are, in turn, divided into well-defined subunits. Phytolaccaceae and Molluginaceae are polyphyletic, and Portulacaceae are paraphyletic, whereas Agdestidaceae, Barbeuiaceae, Petiveriaceae, and Sarcobataceae should be given familial recognition. Two additional lineages are potentially appropriate to be elevated to the family level in the future: the genera Lophiocarpus and Corbichonia form a well-supported clade on the basis of molecular and chemical evidence, and Limeum appears to be separated from other Molluginaceae based on both molecular and ultrastructural data.
Key Words: betalain • Caryophyllales • DNA evolution • matK • phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Eichler, 1876)
. Morphological characters diagnostic of the group include free-central (sometimes basal) placentation, perisperm, and curved embryos (Bittrich, 1993a
). Studies on pigment chemistry (reviewed in Clement et al., 1994
; see also Clement and Mabry, in press
) have shown that all Caryophyllales families, except Caryophyllaceae and Molluginaceae, produce betalain pigments instead of anthocyanins (as is the case in the rest of flowering plants). Studies of the ultrastructure of sieve-element plastids have revealed that Caryophyllales share a unique type (P3; Behnke, 1994
), which is characterized by a peripheral ring of proteinaceous filaments, generally surrounding a protein crystal of either globular or angular shape. Cronquist and Thorne (1994)
, summarizing the data available on Caryophyllales, listed 11 families included in this order: Aizoaceae, Amaranthaceae, Basellaceae, Cactaceae, Caryophyllaceae, Chenopodiaceae, Didiereaceae, Molluginaceae, Nyctaginaceae, Phytolaccaceae, and Portulacaceae. In addition, seven families were excluded: Bataceae, Gyrostemonaceae, Plumbaginaceae, Polygonaceae, Rhabdodendraceae, Theligonaceae, and Vivianaceae.
Molecular systematic studies, starting with Giannasi et al. (1992)
, have substantially increased our knowledge of the phylogeny of the Caryophyllales (Albert, Williams, and Chase, 1992
; Rettig, Wilson, and Manhart, 1992
; Chase et al., 1993
; Downie and Palmer, 1994
; Manhart and Rettig, 1994
; Downie, Katz-Downie, and Cho, 1997
; Fay et al., 1997
; Lledó et al., 1998
; Hoot, Magallón, and Crane, 1999
; Soltis, Soltis, and Chase, 1999
; Meimberg et al., 2000
; Savolainen et al., 2000a, b
; Soltis et al., 2000
; Clement and Mabry, in press
). As a result, additional families have been shown to be related to Caryophyllales: Droseraceae, Drosophyllaceae, Nepenthaceae, Plumbaginaceae, and Polygonaceae (Albert, Williams, and Chase, 1992
; Williams, Albert, and Chase, 1994
), Asteropeiaceae and Physenaceae (Morton, Karol, and Chase, 1997
), Ancistrocladaceae, Dioncophyllaceae, Frankeniaceae, Rhabdodendraceae, Simmondsiaceae, and Tamaricaceae (Fay et al., 1997
). These increasing data led the Angiosperm Phylogeny Group (APG, 1998
) to redefine Caryophyllales to include the families listed above ("noncore Caryophyllales") in addition to those recognized previously ("core Caryophyllales"), a total of 26 families. The closest relatives of Caryophyllales are not yet known with confidence, although Dilleniaceae and perhaps Santalales are the most likely candidates (Hoot, Magallón, and Crane, 1999
; Soltis, Soltis, and Chase, 1999
; Soltis et al., 2000
).
Despite the data available, uncertainties remain as to the delimitation of several families, their phylogenetic relationships, and the placement of some enigmatic genera. Bittrich (1993a)
listed six families that lack clear delimitation or valid synapomorphies: Amaranthaceae, Chenopodiaceae, Portulacaceae, Nyctaginaceae, Phytolaccaceae, and Molluginaceae. Generic composition of Phytolaccaceae, for example, has undergone a continuous thinning, with the recognition of Stegnospermataceae, Achatocarpaceae (as in APG, 1998
), and sometimes also Petiveriaceae, Agdestidaceae, Gisekiaceae, and Barbeuiaceae (Nakai, 1942
) as separate families. A morphological phylogenetic analysis of the order by Rodman et al. (1984)
was criticized by Hershkovitz (1989)
, who wrote that because of several problems (mainly choice of outgroup, definition of taxonomic units, and polymorphic characters within units) the results were less satisfactory than Cronquist's classification (1981)
.
In this paper, we investigate the phylogeny of the order at inter- and infrafamilial levels using partial sequences of the matK plastid gene (sometimes referred to as ORF 542; Hiratsuka et al., 1989
). We also combined these matK sequences with those from plastid rbcL and atpB genes and nuclear 18S rDNA to provide increased support for several deeper branches of the order. In addition, the chemical nature of the red-purple pigments in Corbichonia (Molluginaceae), Lophiocarpus (Phytolaccaceae), and Sarcobatus (Sarcobataceae) is reported here for the first time.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Soltis et al. (2000)
; all available members of the Caryophyllales from the three-gene matrix were included. Alignment of 18S sequences was as in Soltis et al. (2000)
. In a few cases, we could not get all four sequences for the same genus (i.e., the18S rDNA of Trichodiadema is missing, and rbcL, atpB, and 18S rDNA of Stellaria and Mollugo were combined with matK of Moehringia and Pharnaceum, respectively). After comparisons of the published rbcL sequence of Delosperma with those from other Aizoaceae, it was found to be too divergent and doubtful and was therefore deleted from the analyses. In addition, rbcL and atpB were sequenced for Trichodiadema and additional rbcL sequences for the rbcL/matK analysis were retrieved from various sources (see http://ajbsupp.botany.org/).
Taxa, voucher information, and accession numbers of all DNA sequences have been archived at the Botanical Society of America website (http://ajbsupp.botany.org/). Total DNA from fresh, silica gel-dried, or herbarium specimens was extracted using the 2 x cetyltrimethylammonium bromide (CTAB) method of Doyle and Doyle (1987)
and subsequently purified through cesium chloride gradients (see Savolainen et al., 2000a
, for further details). The middle part of matK was amplified by polymerase chain reaction (PCR, 26 cycles, 1-min denaturation at 94°C, 30-sec annealing at 48°C, 1-min extension at 72°C, 7-min final extension) using primers 390F (5'-CGATCTATTCATTCAATATTTC-3') and 1326R (5'-TCTAGCACACGAAAGTCGAAGT-3'), which amplify 930 base pairs between positions 429 and 1313 of the matK sequence of Schmitz-Linneweber et al. (2001)
for Spinacia oleracea L. (these primers appear to be nearly universal for angiosperms). For cases in which amplifications were weak, a second round of PCR (26 cycles) was performed, using 2 µL of the product of the first PCR reaction as template. Amplification products were then purified using QIAquick columns (Qiagen, Crawley, West Sussex, UK). Cycle sequencing (26 cycles, 10-sec denaturation at 96°C, 5-sec annealing at 50°C, 4-min extension at 60°C) with dye terminators was performed in 10 µL volumes and the products were then purified by ethanol precipitation. The redissolved samples were run on a Applied Biosystems 377 automated DNA sequencer following the manufacturer's protocols (Applied Biosystems, Warrington, Cheshire, UK). Both strands were sequenced using the amplification primers, and both sequences overlapped on average for 30% of their overall length. Sequences were aligned manually (there were no particular alignment problems), and the informative indels (12) were coded at the end of the matrix (absent/present). Phylogenetic analysis was performed using PAUP*, version 4.0 (Swofford, 1998
). Parsimony analysis only was performed because previous studies (e.g., Hillis, 1996
) have shown that maximum likelihood tends to agree with parsimony analysis, especially for well-supported groups. Since partition homogeneity tests have shown cases of rejection with no obvious evidence of incongruence (Soltis et al., 2000
; Reeves et al., 2001
), evidence of incongruence was ascertained by examining the levels of bootstrap percentages of the groups in the combined analysis relative to the separate analyses. The specific issue of combining 18S rDNA and plastid DNA gene sequences for analyses of these angiosperms has been adequately covered previously in Soltis et al. (2000)
.
Most-parsimonious trees were obtained using 1000 replicates of random taxon addition with equal weights and tree-bisection-reconnection (TBR) branch swapping, with only 50 trees held at each replicate to reduce time spent in searching nonoptimal tree lengths. Using only the matK matrix, heuristic searches did not swap to completion, therefore only 10 000 of the trees found in 200 independent replicates were retained for discussion. Internal support was assessed using 1000 bootstrap replicates with TBR swapping and simple addition of taxa, with a limit of ten trees kept in each replicate.
For calculation of substitution patterns, nucleotide changes for each of the four genes were optimized with ACCTRAN onto the four-gene tree (Delosperma being excluded for the plastid genes). Sequences of the three coding genes were translated into amino acids using MacClade 3.04 (Maddison and Maddison, 1992
), and the amino acid changes were computed after optimization onto the combined tree.
For chemical analysis of pigments, 10–50 mg of dried stems of Sarcobatus vermiculatus Torr., Corbichonia decumbens (Forsk.) Exell, Adenogramma sp., and Lophiocarpus polystachyus Turcz. were cut into small pieces and extracted for 5 min in boiling 50% aqueous methanol. The extracts were cooled, filtered, and evaporated to dryness at 40°C under vacuum. The precipitates were dissolved in two drops of distilled water, and 0.5 mL of 80% aqueous methanol was added to this solution. Extracts of fresh red leaves of Iresine sp. (Amaranthaceae; containing betacyanins) and Papaver sp. (Papaveraceae; containing anthocyanins) were prepared in a similar way and used for comparison. The extracts were analyzed for the presence of anthocyanins or betacyanins in two ways. First, we used reverse-phase, high-performance liquid chromatography (HPLC) with diode array detection (40 µL injections) to assess the polarity and uv/visible spectrum of any pigment present. The HPLC equipment used (Waters Ltd., Watford, UK) consisted of a model LC600 pump coupled with a model 996-photodiode array detector controlled by Millennium software (Column Merck Lichrospher 100RP-18, 250 x 4.0 mm internal diameter; 5 µm particle size; temperature of the column was maintained at 30°C). Elution was performed with a linear gradient of two solvents: 2% aqueous acetic acid (solvent A) and methanol : acetic acid : water (18:1:1; solvent B), starting with 25% B and changing to 100% B over 20 min, followed by isocratic elution with 100% B. The diode-array detector was set to record uv/visible spectra of all eluting compounds between 200 and 600 nm. Second, we added two drops of 2 mol/L potassium hydroxide (KOH) to the crude extract to see the color reaction; development of a blue color with KOH indicates presence of anthocyanins and of a yellow color the presence of betacyanins (Harborne, 1998
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; see Table 1 for taxon coverage within families) plus 13 for members of the putative outgroups Dilleniaceae, Olacaceae, Santalaceae, and Opiliaceae (only the first half of this sequence could be obtained for Adenogramma, but this was enough to place this taxon with 100% bootstrap support). After alignment, the matrix contained 1013 characters, of which 30 at the 5' end and 52 at the 3' end were trimmed to limit the amount of missing data in the matrix. An additional stretch of 12 nucleotides was excluded, corresponding to two insertions in one outgroup and one ingroup taxon, because of dubious homology. Twelve potentially informative indels were coded at the end of the matrix if they shared same position and size (all indels were in sets of three). No stop codons were found when the sequences were translated into amino acids. In three species belonging to Caryophyllaceae (i.e., Silene italica Pers., Paronychia sp., and Arenaria tetraquetra L.), highly divergent matK sequences were recovered; these clustered within the monocots (with low similarity) in parsimony analyses including a broad sampling of angiosperms (L. W. Chatrou et al., unpublished data). The presence of these "anomalous" sequences is not lineage specific because another matK sequence was retrieved from another Silene species, S. rothmaleri Pinto da Silva, which matched the other sequences in Caryophyllales. The "anomalous" sequences have not been included in the matrix because they would have given only spurious results.
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Within core Caryophyllales (75% BS), Asteropeia is sister to the rest of the taxa (100% BS). Caryophyllaceae form a well-supported clade (100% BS), which is sister to the rest of the core Caryophyllales (BS < 50%). A clade grouping Amaranthaceae and Achatocarpaceae (57% BS) is sister to the rest of core Caryophyllales (62% BS). Another large clade (92% BS) includes Nyctaginaceae and Aizoaceae (both recovered as monophyletic; 85 and 97% BS, respectively), as well as genera attributed to Phytolaccaceae, Molluginaceae, and Sarcobatus, Gisekia, Barbeuia (Barbeuiaceae), and Agdestis. Nyctaginaceae are sister to Sarcobatus (with BS < 50%), as is the case for Aizoaceae and Gisekia (52% BS). The members of Rivinoideae (Phytolaccaceae) form another monophyletic group supported by 97% BS, also associated with Agdestis (59% BS). Phytolaccaceae s.s. (Phytolacca and Ercilla) form another monophyletic group supported by 100% BS, which is sister to the Nyctaginaceae/Sarcobatus/Rivinoideae/Agdestis group (96% BS). Barbeuia is sister to this clade (59% BS) and the pair Corbichonia, and Lophiocarpus is sister to Barbeuia and this clade (95% BS for the clade, 92% BS for its placement). The last large clade (88% BS) contains a subclade of genera attributed to Molluginaceae (89% BS) plus a clade composed of Cactaceae, Portulacaceae, Basellaceae, Didiereaceae, and Halophytum (97% BS). Cactaceae, Basellaceae, and Didiereaceae are monophyletic (72, 99, and 90% BS, respectively). Calyptrotheca is associated with Didiereaceae (68% BS), and four genera or groups of genera attributed to Portulacaceae are identified.
Finally, there are two "soft" incongruences (Seelanan, Schnabel, and Wendel, 1997
) between the matK and the combined analyses described above, i.e., the association of Rhabdodendron and Simmondsia as sister groups and the position of Amaranthaceae (compare Figs. 1 and 3b), but none of these placements receives BS > 50%. We therefore attribute these to sampling error, not true incongruence (Huelsenbeck, Bull, and Cunningham, 1996
).
Chemical analysis of pigments
Addition of KOH to the dark red Papaver extract, used as the anthocyanin source, turned its color to blue, as expected for anthocyanins. This color slowly faded within a day. Addition of KOH to the dark or pink-red Iresine, Sarcobatus, Corbichonia, and Lophiocarpus extracts turned them to bright yellow, indicating presence of betacyanins. These colors did not fade even after a week. The HPLC of the Iresine, Corbichonia, and Lophiocarpus extracts revealed presence of one or two compounds in each extract that absorbed visible light at 536 nm in aqueous methanol/acetic acid. All these compounds had short retention times (2.1–2.2 min), indicating that they are polar. The extract of Sarcobatus contained three compounds absorbing visible light at 536 nm in aqueous methanol/acetic acid, with retention times of 2.2, 11.1, and 11.4 min, respectively. The compounds with longer retention times not only absorbed visible light but also uv at 299 and 326 nm. The Papaver extract contained five compounds with absorbance in both the visible and uv range. Their retention times were 8.2, 10.4, 11.4, 15.3, and 16.2 min, and the 
max (in nanometers) of their uv/visible spectra in aqueous methanol/acetic acid were 277–517, 283–517, 283–523, 283–523, and 283–523, respectively. The Adenogramma sample failed to produce pigments of either the betacyanin or anthocyanin class.
Because betacyanins are in general polar compounds, they usually have short retention times using reversed phased HPLC. Many betacyanins only absorb visible light (at 536 nm) and not uv. Anthocyanins, on the other hand, are less polar, and therefore have longer retention times; they absorb both uv and visible light (Harborne, 1998
). The visible max of red-colored anthocyanins is at a shorter wavelength than that of betacyanins (e.g., 523 nm for red cyanidin glycosides, but ranging from 505 to 535 nm for orange-red to blue anthocyanins). However, some species of Caryophyllales contain betacyanins with complex side chains containing phenolic acids, e.g., Christmas cactus (Schlumbergera x buckleyi), and these pigments have retention times like those of anthocyanins and absorb uv as well as visible light (Kobayashi et al., 2000
). However, their max in visible light (537–549 nm) is always longer than that of anthocyanins. Using the above criteria, it is clear that Sarcobatus, Corbichonia, and Lophiocarpus all contain betacyanins rather than anthocyanins. Two of the betacyanins in Sarcobatus seem to have complex attachments because they absorb uv and have relatively long retention times.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Of the protein-coding genes, matK has a high proportion of nonsynonymous change (the amino acid changes/nucleotide substitutions ratio is 0.53 for matK, compared with 0.23 and 0.32 for rbcL and atpB, respectively). Although the number of changes at third codon position is similar across genes (Fig. 4), matK has a distinctively higher rate of change at the first and second positions, indicating that although all genes have a similar rate of neutral change, matK has an apparently higher rate of amino acid change. Because matK is more variable than the other genes but has similar CI and RI values, we conclude that it has a higher number of similarly informative characters. For matK alone, 21 clades received BS > 50%, whereas there was a total of only 28 for the four-gene combined matrix (Table 3).
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; Chase et al., 1993
; Nandi, Chase, and Endress, 1998
).
The positions of Simmondsia and especially Rhabdodendron lack strong support (see Fig. 3b). Their respective placements received weaker BS in the four-gene analysis (73 and 50%, respectively), compared to 18S rDNA/rbcL/atpB combined (79 and 69%, respectively), indicating that matK does not bring additional support for the placement of these taxa. The position of these two taxa as sister groups in the matK analysis is probably due to sampling error, given evidence derived from combined analyses; this association was also found in some of the shortest trees inferred from atpB sequences (Savolainen et al., 2000b)
, presumably for the same reason.
Core Caryophyllales
The combined data sets gave substantial support for the division of this group (minus Asteropeia) into two sister clades. The first clade includes Nyctaginaceae, Phytolaccaceae, Aizoaceae, Molluginaceae, Cactaceae, Portulacaceae, Stegnospermataceae, and several rather isolated genera. This clade has been shown by Clement and Mabry (in press)
to share the derived character of a globular crystal in sieve-element plastids for all taxa except Limeum and Stegnosperma, which have an angular inclusion. Unlike their results, our data indicate that Limeum is sister to the rest of this clade (minus Stegnosperma), thus matching the distribution of sieve-element plastids. Another observation made by Clement and Mabry (in press)
is that taxa possessing anthocyanins (Molluginaceae and Caryophyllales) are present in both of the two main clades within core Caryophyllales, thus showing that the betalain-producing families are not monophyletic. Our results show two anthocyanin-producing taxa, Molluginaceae (minus Corbichonia and Limeum) and Caryophyllaceae, are nested within the betalain-producing clades. Limeum, which appears as sister to a group of taxa producing both anthocyanins and betalains, possesses none of these pigments (Clement et al., 1994
).
Aizoaceae, Nyctaginaceae, and Phytolaccaceae are characterized by the presence of raphide crystals (Judd et al., 1999
). Aizoaceae appear to be monophyletic based on the matK analysis, with Ruschioidae (here represented by Delosperma, Phyllobolus, Ruschia, and Trichodiadema) forming a clade sister to Aizooidae (Galenia and Plinthus). With Gisekia, the family is sister to a clade including principally Phytolaccaceae s.l. and Nyctaginaceae. This differs from several studies based on rbcL alone; in Savolainen et al. (2000a)
, in which Trianthema (Sesuvioidae) and Delosperma were represented, only the former occupied a similar position to our analysis, whereas the latter was nested within Phytolaccaceae s.s. (as specified in the MATERIALS AND METHODS section, we did not include the Delosperma sequence for rbcL in this paper because we judged it too divergent from other rbcL sequences of Aizoaceae and hence doubtful). In Clement and Mabry's study (in press)
, in which all subfamilies were sampled (but Delosperma was not included), the family formed a grade at the base of Phytolaccaceae/Nyctaginaceae. However, monophyly of Aizoaceae has not generally been challenged in the literature (e.g., Bittrich, 1993a
).
The position of Gisekia as sister to Aizoaceae (according to matK) is surprising because analyses using rbcL sequence in Manhart and Rettig (1994)
indicated a strong affinity with Rivina (Phytolaccaceae, Rivinoidae). Our combined rbcL/matK analysis placed Gisekia within Rivinoideae, thereby indicating that matK alone is possibly misleading with respect to this taxon. Nyctaginaceae appear to be monophyletic, with the Nyctagineae (Allionia, Boerhavia, Commicarpus, Mirabilis, Oxybaphus, Selinocarpus) forming a clade to the exclusion of Bougainvillea (Bougainvilleae) and Pisonia (Pisonieae).
Sarcobatus was separated from Chenopodiaceae by Behnke (1997)
on the basis of its sieve-element plastids. This genus has been shown by Downie, Katz-Downie, and Cho (1997)
to be associated with Nyctaginaceae/Phytolaccaceae s.l. based on the analysis of ORF2280 sequences. Clement and Mabry (in press)
, using rbcL sequences, found that Sarcobatus and Agdestis formed a clade sister to Nyctaginaceae-Rivinoideae, whereas, according to matK (in this paper), Sarcobatus is sister to Nyctaginaceae, and Agdestis is sister to Rivinoideae. The presence of betacyanins in Sarcobatus as reported here compares well with the phylogenetic pattern since this genus is nested within betalain-producing families.
The three subfamilies of Phytolaccaceae (if one excludes Agdestis and Barbeuia from this family) do not appear directly related to each other. The monocarpellate Rivinoideae (represented here by Gallesia, Hilleria, Ledenbergia, Petiveria, Rivina, and Seguieria) form a monophyletic group more closely related to Nyctaginaceae (with which they share a monocarpellate gynoecium) than to Phytolaccaceae s.s. Petiveria and Gallesia, which are sister in our analyses, share a strong garlic smell (Rohwer, 1993
). Phytolaccaceae s.s. (represented here by Phytolacca and Ercilla) are sister to Nyctaginaceae/Rivinoideae/Sarcobatus/Agdestis, which is in agreement with the rbcL study of Clement and Mabry (in press)
.
Madagascan, monotypic Barbeuia was said by Rohwer (1993)
to be of "completely obscure" affinities because of divergent characters (i.e., semi-arillate seeds and capsular fruits). Based on matK, Barbeuia is outside the Aizoaceae/Nytaginaceae/Phytolaccaceae clade, which indicates a rather isolated position for this taxon. More sequence data for Barbeuia would be of great interest, and, given its position, data about pigment nature would be of special relevance.
The sister group relationship of Corbichonia (previously placed in Molluginaceae) and the South African genus Lophiocarpus (Phytolaccaceae, Microteoideae) was unpredicted. Rohwer (1993)
emphasized the differences between the two genera from Microteoideae (Lophiocarpus and Microtea) and the rest of Phytolaccaceae; however, he suggested affinities with Chenopodiaceae (particularly Microtea, for which sieve-element plastids lack a central inclusion). Behnke (1994)
showed that Lophiocarpus has the same type of plastid (i.e., P3 with a globular crystal) as some Molluginaceae; Corbichonia has not been studied in this respect. Clement and Mabry (in press)
showed a relationship of Corbichonia with Aizoaceae/Nyctaginaceae/Phytolaccaceae in agreement with our study, and the rbcL/matK combined analysis gave a similar position to Corbichonia as with matK alone (no rbcL sequence was available for Lophiocarpus). The presence of betacyanins in Corbichonia, as reported in this paper, is an indication that this genus is probably misplaced among Molluginaceae. Because we showed that Lophiocarpus also contains betacyanins, this might be considered as additional evidence for Corbichonia and Lophiocarpus to constitute a separate lineage that may ultimately be considered a new family.
The clade formed by Cactaceae, Portulacaceae, Basellaceae, Didiereaceae, and Halophytum was named the "succulent" clade by Manhart and Rettig (1994)
. Non-DNA characters that define it include the presence of an involucre (in Didiereaceae, Basellaceae, and Portulacaceae) and normal secondary growth (not always in Cactaceae). The paraphyly of Portulacaceae has long been suspected (see Carolin, 1987
, 1993
). However, the matK analysis suffers from a lack of support with respect to this group. Five portulacaceous genera (Calandrinia, Cistanthe, Claytonia, Lewisia, and Montia) form a clade, all Didiereaceae genera are grouped with Calyptrotheca, Basella/Anredera are sometimes sister to Portulacaria, all Cactaceae sampled (Opuntia, Pereskia, Quiabentia, Rhipsalis, and Tacinga) are grouped together with Portulaca (but with BS < 50%), and Talinaria is sister to Anacampseros. Hence, the only supported evidence of paraphyly for Portulacaceae is the grouping of Calyptrotheca with Didiereaceae (68% BS), which corresponds to the findings of Applequist and Wallace (2000)
, which were based on an rpl16/trnL-F/trnT-L combined analysis. The phylogenetic relationships of Didiereaceae as inferred from matK, with Alluaudiopsis as sister to the remaining three genera (which appear in an unresolved trichotomy), are identical to the results of Applequist and Wallace (2000)
.
The grouping of the five genera from Portulacaceae corresponds to what Hershkovitz (1993)
identified as the "west American group" on the basis of morphological characters (see also Hershkovitz and Zimmer, 2000
). Moreover, the affinities of Talinaria and Anacampseros have been outlined by Hershkovitz (1993)
and Hershkovitz and Zimmer (1997)
. Within Cactaceae, genera belonging to Opuntioideae (Opuntia, Tacinga, and Quiabentia) form a well-supported clade. The position of Halophytum in the portulacaceous clade is congruent with analyses of rbcL sequences that supported a sister group relationship of Halophytum with Basellaceae (Savolainen et al., 2000a
). Such a relationship appears only in some of the most parsimonious matK trees. Possible relatedness of Halophytum to Basellaceae was suggested by Bittrich (1993b)
because of their similar cuboidal pollen grains and by Hunziker, Pozner, and Escobar (2000)
because of their similar chromosome numbers.
According to our analysis, taxa formerly included in Chenopodiaceae (i.e., Atriplex, Axyris, Beta, Blackiella, Chenopodium, Hablitzia, Kochia, Maireana, Rhagodia, Suaeda, and Spinacia) form a monophyletic group in some of shortest trees only, whereas genera formerly included in Amaranthaceae s.s. (i.e., Achyranthes, Alternanthera, Amaranthus, Bosea, Celosia, Froelichia, Gomphrena, Iresine, Psilotrichum, and Ptilotus) form a well-supported clade (97% BS). Using sequences of ORF 2280, Downie, Katz-Downie, and Cho (1997)
found a lack of separation between the two families (although they did not find members of Amaranthaceae s.s. forming a clade), and for similar reasons APG (1998)
included Chenopodiaceae within Amaranthaceae s.l. In addition, we found Beteae to be monophyletic (Beta and Hablitzia) and distinct from a clade comprising various genera from Atripliceae/Chenopodieae (Atriplex, Axyris, Blackiella, Chenopodium, Rhagodia, and Spinacia). The association of Amaranthaceae s.l. with the Neotropical family Achatocarpaceae (Achatocarpus and Phaulothamnus) agrees with Manhart and Rettig's results (1994)
.
Although Caryophyllaceae are placed as sister to the rest of the core Caryophyllales in the matK analysis, they are more likely to be part of the Amaranthaceae/Achatocarpaceae clade, as found in the combined analyses (Fig. 1). Based on the genera we sampled, the separation into three subfamilies is not supported, with Paronychoideae (here represented by Telephium, sometimes included in Molluginaceae) as sister to mixed members of Alsinoideae (Honckenya and Moehringia) and Caryophylloideae (Lychnis, Silene, Vaccaria, Saponaria, and Gypsophila).
Because Molluginaceae lack clear synapomorphies (Bittrich, 1993a
; Endress and Bittrich, 1993
), Clement and Mabry (in press)
wrote that "there is no obvious reason to expect the family to appear as a clade." In the matK alone analysis, the six genera we sampled to represent this family appeared in three different positions, showing no apparent congruence with the classification of Hofmann (1973)
. Adenogramma, Glischrothamnus, Glinus, Pharnaceum, and Suessenguthiella are sister to the "succulent" clade and may constitute the best candidate for a redefined, monophyletic Molluginaceae. Corbichonia is sister to Lophiocarpus, and both together are sister to Aizoaceae/Phytolaccaceae/Nyctaginaceae. Limeum is sister to the "globular inclusion" clade in the combined four-gene analyses (Fig. 1), whereas its position is unresolved using matK alone (Fig. 3c). Since Limeum possesses a different type of sieve-element plastid inclusion, it represents most probably a separate lineage from the remaining Molluginaceae and could deserve familial status. The Australian genus Macarthuria possesses the same type of sieve-element plastid (Behnke, 1994
) and might be sister to Limeum, but we have no DNA sequence data for this genus yet.
Noncore Caryophyllales
The monophyly of this group, although not supported by some studies based on rbcL (e.g., Savolainen et al., 2000a
), is well established by the combined analysis. Diagnostic characters for this clade include: secretory cells containing plumbagin, stalked, gland-headed hairs, basal placentation, and starchy endosperm (Judd et al., 1999
), although some of these have been lost in one or more lineages.
All carnivorous families of Caryophyllales (Droseraceae, Drosophyllaceae, Nepenthaceae, Dioncophyllaceae), along with Ancistrocladaceae, form a monophyletic group based on the matK analysis. All carnivorous syndromes except for the bladders found in Utricularia are present in this group (fly-paper traps in Drosera, Drosophyllum, and Triphyophyllum, traps in Aldrovanda and Dionaea, and pitchers in Nepenthes). The west African endemic Triphyophyllum peltatum Airy Shaw (Dioncophyllaceae) provides a possible link between syndromes: it produces glandular, sticky hairs (in a similar manner to Drosera and Drosophyllum) in its juvenile stage, whereas its adult stage, a vine with apical leaf-tendrils, is reminiscent of Nepenthes without pitchers (Albert, Williams, and Chase, 1992
). The evolution of carnivory in the Caryophyllales group has been reviewed in detail in Meimberg et al. (2000)
.
Frankeniaceae are sister to Tamaricaceae, with which they share many similarities; e.g., heath-like shrubby habit in some species, capsular fruit, and straight embryo (Heywood, 1993
), but it is not possible to tell if one family is nested in the other one with only the current information in which one genus was sampled per family. The proximity of Plumbaginaceae to Polygonaceae is well supported, and the clade they form is the best resolved of all analyses. Within Plumbaginaceae, the dichotomy between Plumbaginoideae (Dyerophyton, Plumbago, and Ceratostigma) and Staticoideae (Afrolimon, Armeria, Goniolimon, Limoniastrum, Limonium, and Psylliostachys) is clearly established, as was already shown based on rbcL (Lledó et al., 1998
). The situation is less clear in Polygonaceae, in which not all of the groupings we found correspond to previously recognized entities. Triplareae (genera Triplaris and Ruprechtia) appear to be well supported, as do Rumiceae (Emex, Rumex, Oxyria, and Rheum), whereas Persicarieae (Koenigia, Persicaria, Bistorta, and Fagopyrum), Coccolobeae (Brunnichia, Coccoloba, and Muehlenbeckia), and the pentamerous-flowered Polygoneae (Polygonum and Fallopia) are poly- or paraphyletic.
Despite the fact that we used only a small portion of the matK exon, this DNA region contains enough variable sites to resolve many infrafamilial relationships within Caryophyllales, its high variability corresponding to high phylogenetic content. However, although a great deal of progress has been made lately, the definition of all natural entities within Caryophyllales is not yet fully satisfactory. This phylogenetic study presents evidence for the recognition of Agdestidaceae, Barbeuiaceae, Petiveriaceae, and Sarcobataceae, and Limeum, and the pair Corbichonia/Lophiocarpus may be ultimately recognized as separate families. The genus Halophytum is definitely not part of Amaranthaceae, but it is difficult to determine if it deserves familial status or should be included, for example, in Basellaceae. The systematics of the "succulent" clade are especially in need of revision, with perhaps the recognition of an expanded family Cactaceae that could include portulacaceous genera such as Portulaca, Anacampseros, or Talinum (Hershkowitz and Zimmer, 1997
). Molluginaceae, excluding Limeum and Corbichonia, appear well defined, but some genera (e.g., Macarthuria and Polpoda) have not been sampled yet for DNA work.
Ehrendorfer (1976)
provided an hypothesis to explain the presence of betalains in Caryophyllales. According to his ideas, ancestral taxa of the group may have evolved in dry environments on mineral substrates with a tendency towards anemophily; having lost the need to attract pollinators, they would have also lost the ability to synthesize anthocyanin pigments. If this is true, betalain synthesis may have evolved during subsequent reversals to zoochory. Interestingly, Limeum, which is unpigmented (Clement et al., 1994
), comes as sister to the "globular inclusion" clade that produces both betalain and anthocyanin, but the anthocyanin-producing taxa are nested among betalain-producing ones. Another interesting case is that of Caryophyllaceae (producing anthocyanins) that are associated with Amaranthaceae (producing betalains) and Achatocarpaceae, for which the nature of pigments is not known (Clement et al., 1994
). Although we are far from fully understanding the evolution of all peculiarities in Caryophyllales, phylogenetic data are increasing rapidly and will lead to substantial progress in the near future. As Ehrendorfer (1976)
put it, "the evolutionary picture emerging for the Centrospermae families differentiating and radiating in time and space is one of the most fascinating in the plant kingdom."
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FOOTNOTES |
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5 Author for reprint requests (philcuenoud_68{at}hotmail.com
).
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G. J. Jordan and M. K. Macphail A Middle-Late Eocene inflorescence of Caryophyllaceae from Tasmania, Australia Am. J. Botany, May 1, 2003; 90(5): 761 - 768. [Abstract] [Full Text] [PDF]
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G. A. Salazar, M. W. Chase, M. A. Soto Arenas, and M. Ingrouille Phylogenetics of Cranichideae with emphasis on Spiranthinae (Orchidaceae, Orchidoideae): evidence from plastid and nuclear DNA sequences Am. J. Botany, May 1, 2003; 90(5): 777 - 795. [Abstract] [Full Text] [PDF]
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M. R. Broadley, H. C. Bowen, H. L. Cotterill, J. P. Hammond, M. C. Meacham, A. Mead, and P. J. White Variation in the shoot calcium content of angiosperms J. Exp. Bot., May 1, 2003; 54(386): 1431 - 1446. [Abstract] [Full Text] [PDF]
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K. Yamane, Y. Yasui, and O. Ohnishi Intraspecific cpDNA variations of diploid and tetraploid perennial buckwheat, Fagopyrum cymosum (Polygonaceae) Am. J. Botany, March 1, 2003; 90(3): 339 - 346. [Abstract] [Full Text] [PDF]
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A. N. Muellner, R. Samuel, S. A. Johnson, M. Cheek, T. D. Pennington, and M. W. Chase Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences Am. J. Botany, March 1, 2003; 90(3): 471 - 480. [Abstract] [Full Text] [PDF]
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K. M. Cameron, K. J. Wurdack, and R. W. Jobson Molecular evidence for the common origin of snap-traps among carnivorous plants Am. J. Botany, September 1, 2002; 89(9): 1503 - 1509. [Abstract] [Full Text] [PDF]
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