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Molecular Phylogenetics of Caryophyllales Based on Nuclear 18S Rdna and Plastid Rbcl, Atpb, and Matk Dna Sequences1

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Molecular Phylogenetics of Caryophyllales Based on Nuclear 18S Rdna and Plastid Rbcl, Atpb, and Matk Dna Sequences1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Ghent University Academic Bibliography American Journal of Botany 89(1): 132±144. 2002. MOLECULAR PHYLOGENETICS OF CARYOPHYLLALES BASED ON NUCLEAR 18S RDNA AND PLASTID RBCL, ATPB, AND MATK DNA SEQUENCES1 PHILIPPE CUE NOUD,2,5 VINCENT SAVOLAINEN,2 LARS W. C HATROU,3 MARTYN POWELL,2 RENE E J. GRAYER,4 AND MARK W. C HASE2 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 To study the inter- and infrafamilial phylogenetic relationships in the order Caryophyllales sensu lato (s.l.), ;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-de®ned subunits. Phytolaccaceae and Molluginaceae are polyphyletic, and Por- tulacaceae are paraphyletic, whereas Agdestidaceae, Barbeuiaceae, Petiveriaceae, and Sarcobataceae should be given familial recog- nition. 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. Caryophyllales sensu stricto (s.s), sometimes also called Downie and Palmer, 1994; Manhart and Rettig, 1994; Downie, Centrospermae, have long been identi®ed as a natural assem- Katz-Downie, and Cho, 1997; Fay et al., 1997; Lledo et al., blage of families (Braun, 1864; Eichler, 1876). Morphological 1998; Hoot, MagalloÂn, and Crane, 1999; Soltis, Soltis, and characters diagnostic of the group include free-central (some- Chase, 1999; Meimberg et al., 2000; Savolainen et al., 2000a, times basal) placentation, perisperm, and curved embryos (Bit- b; Soltis et al., 2000; Clement and Mabry, in press). As a trich, 1993a). Studies on pigment chemistry (reviewed in result, additional families have been shown to be related to Clement et al., 1994; see also Clement and Mabry, in press) Caryophyllales: Droseraceae, Drosophyllaceae, Nepenthaceae, have shown that all Caryophyllales families, except Cary- Plumbaginaceae, and Polygonaceae (Albert, Williams, and ophyllaceae and Molluginaceae, produce betalain pigments in- Chase, 1992; Williams, Albert, and Chase, 1994), Asteropei- stead of anthocyanins (as is the case in the rest of ¯owering aceae and Physenaceae (Morton, Karol, and Chase, 1997), An- plants). Studies of the ultrastructure of sieve-element plastids cistrocladaceae, Dioncophyllaceae, Frankeniaceae, Rhabdod- have revealed that Caryophyllales share a unique type (P3; endraceae, Simmondsiaceae, and Tamaricaceae (Fay et al., Behnke, 1994), which is characterized by a peripheral ring of 1997). These increasing data led the Angiosperm Phylogeny proteinaceous ®laments, generally surrounding a protein crys- Group (APG, 1998) to rede®ne Caryophyllales to include the tal of either globular or angular shape. Cronquist and Thorne families listed above (``noncore Caryophyllales'') in addition (1994), summarizing the data available on Caryophyllales, list- to those recognized previously (``core Caryophyllales''), a to- ed 11 families included in this order: Aizoaceae, Amarantha- tal of 26 families. The closest relatives of Caryophyllales are ceae, Basellaceae, Cactaceae, Caryophyllaceae, Chenopodi- not yet known with con®dence, although Dilleniaceae and per- aceae, Didiereaceae, Molluginaceae, Nyctaginaceae, Phytolac- haps Santalales are the most likely candidates (Hoot, Magal- caceae, and Portulacaceae. In addition, seven families were loÂn, and Crane, 1999; Soltis, Soltis, and Chase, 1999; Soltis excluded: Bataceae, Gyrostemonaceae, Plumbaginaceae, Poly- et al., 2000). gonaceae, Rhabdodendraceae, Theligonaceae, and Viviana- Despite the data available, uncertainties remain as to the ceae. delimitation of several families, their phylogenetic relation- Molecular systematic studies, starting with Giannasi et al. ships, and the placement of some enigmatic genera. Bittrich (1992), have substantially increased our knowledge of the phy- (1993a) listed six families that lack clear delimitation or valid logeny of the Caryophyllales (Albert, Williams, and Chase, synapomorphies: Amaranthaceae, Chenopodiaceae, Portula- 1992; Rettig, Wilson, and Manhart, 1992; Chase et al., 1993; caceae, Nyctaginaceae, Phytolaccaceae, and Molluginaceae. 1 Manuscript received 22 February 2001; revision accepted 27 July 2001. Generic composition of Phytolaccaceae, for example, has un- The authors thank James R. Manhart, who provided DNA of Phaulotham- dergone a continuous thinning, with the recognition of Steg- nus; Wendy L. Applequist, who provided most of the Portulacaceae samples, nospermataceae, Achatocarpaceae (as in APG, 1998), and as well as leaf tissue of Alluaudiopsis; Tom J. Mabry, who provided a copy sometimes also Petiveriaceae, Agdestidaceae, Gisekiaceae, and of his paper in press; and the late Patricia Geissler for her help in getting Barbeuiaceae (Nakai, 1942) as separate families. A morpho- funding for this study. This study was funded by the Royal Botanic Gardens, Kew, the Royal Society (London), the Swiss NSF (31-52378.97), and the logical phylogenetic analysis of the order by Rodman et al. Academic Society of Geneva. (1984) was criticized by Hershkovitz (1989), who wrote that 5 Author for reprint requests (e-mail: [email protected]). because of several problems (mainly choice of outgroup, def- 132 January 2002] CUE NOUD ET AL.ÐMOLECULAR PHYLOGENETICS OF CARYOPHYLLALES 133 inition of taxonomic units, and polymorphic characters within taxon addition with equal weights and tree-bisection-reconnection (TBR) units) the results were less satisfactory than Cronquist's clas- branch swapping, with only 50 trees held at each replicate to reduce time si®cation (1981). spent in searching nonoptimal tree lengths. Using only the matK matrix, heu- In this paper, we investigate the phylogeny of the order at ristic searches did not swap to completion, therefore only 10 000 of the trees inter- and infrafamilial levels using partial sequences of the found in 200 independent replicates were retained for discussion. Internal matK plastid gene (sometimes referred to as ORF 542; Hira- support was assessed using 1000 bootstrap replicates with TBR swapping and tsuka et al., 1989). We also combined these matK sequences simple addition of taxa, with a limit of ten trees kept in each replicate. with those from plastid rbcL and atpB genes and nuclear 18S For calculation of substitution patterns, nucleotide changes for each of the rDNA to provide increased support for several deeper branch- four genes were optimized with ACCTRAN onto the four-gene tree (Delos- es of the order. In addition, the chemical nature of the red- perma being excluded for the plastid genes). Sequences of the three coding purple pigments in Corbichonia (Molluginaceae), Lophiocar- genes were translated into amino acids using MacClade 3.04 (Maddison and Maddison, 1992), and the amino acid changes were computed after optimi- pus (Phytolaccaceae), and Sarcobatus (Sarcobataceae) is re- zation onto the combined tree. ported here for the ®rst time. For chemical analysis of pigments, ;10±50 mg of dried stems of Sarcobatus vermiculatus Torr., Corbichonia decumbens (Forsk.) Exell, Adenogramma sp., MATERIALS AND METHODS and Lophiocarpus polystachyus Turcz. were cut into small pieces and extracted Sequences of the rbcL and atpB exons and 18S rDNA were taken from the for 5 min in boiling 50% aqueous methanol. The extracts were cooled, ®ltered, studies of Soltis, Soltis, and Chase (1999) and Soltis et al. (2000); all available and evaporated to dryness at 408C under vacuum. The precipitates were dis- members of the Caryophyllales from the three-gene matrix were included. solved in two drops of distilled water, and 0.5 mL of 80% aqueous methanol Alignment of 18S sequences was as in Soltis et al. (2000). In a few cases, was added to this solution. Extracts of fresh red leaves of Iresine sp. (Amar- we could not get all four sequences for the same genus (i.e., the18S rDNA anthaceae; containing betacyanins) and Papaver sp. (Papaveraceae; containing of Trichodiadema is missing, and rbcL, atpB, and 18S rDNA of Stellaria and anthocyanins) were prepared in a similar way and used for comparison. The Mollugo were combined with matK of Moehringia and Pharnaceum, respec- extracts were analyzed for the presence of anthocyanins or betacyanins in two tively). After comparisons of the published rbcL sequence of Delosperma with ways. First, we used reverse-phase, high-performance liquid chromatography those from other Aizoaceae, it was found to be too divergent and doubtful (HPLC)
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