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Saxifragaceae Sensu Lato (DNA Sequencing/Evolution/Systematics) DOUGLAS E

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Saxifragaceae Sensu Lato (DNA Sequencing/Evolution/Systematics) DOUGLAS E Proc. Nati. Acad. Sci. USA Vol. 87, pp. 4640-4644, June 1990 Evolution rbcL sequence divergence and phylogenetic relationships in Saxifragaceae sensu lato (DNA sequencing/evolution/systematics) DOUGLAS E. SOLTISt, PAMELA S. SOLTISt, MICHAEL T. CLEGGt, AND MARY DURBINt tDepartment of Botany, Washington State University, Pullman, WA 99164; and tDepartment of Botany and Plant Sciences, University of California, Riverside, CA 92521 Communicated by R. W. Allard, March 19, 1990 (received for review January 29, 1990) ABSTRACT Phylogenetic relationships are often poorly quenced and analyses to date indicate that it is reliable for understood at higher taxonomic levels (family and above) phylogenetic analysis at higher taxonomic levels, (ii) rbcL is despite intensive morphological analysis. An excellent example a large gene [>1400 base pairs (bp)] that provides numerous is Saxifragaceae sensu lato, which represents one of the major characters (bp) for phylogenetic studies, and (iii) the rate of phylogenetic problems in angiosperms at higher taxonomic evolution of rbcL is appropriate for addressing questions of levels. As originally defined, the family is a heterogeneous angiosperm phylogeny at the familial level or higher. assemblage of herbaceous and woody taxa comprising 15 We used rbcL sequence data to analyze phylogenetic subfamilies. Although more recent classifications fundamen- relationships in a particularly problematic group-Engler's tally modified this scheme, little agreement exists regarding the (8) broadly defined family Saxifragaceae (Saxifragaceae circumscription, taxonomic rank, or relationships of these sensu lato). Based on morphological analyses, the group is subfamilies. The recurrent discrepancies in taxonomic treat- almost impossible to distinguish or characterize clearly and ments of the Saxifragaceae prompted an investigation of the taxonomic problems at higher power of chloroplast gene sequences to resolve phylogenetic represents one of the greatest relationships within this family and between the Saxifragaceae levels in the angiosperms (9, 10). Following the traditional and other major plant lineages. Sequence data from the gene interpretation (8), the family is a large, morphologically rbcL (ribulose-1,5-bisphosphate carboxylase, large subunit) diverse assemblage of annual, biennial, and perennial herbs, reveal that (i) Saxifragaceae sensu lato is at least paraphyletic, shrubs, trees, and vines comprising 15 subfamilies; this was and probably polyphyletic, (ii) the generaParnassia andBrexia later increased to 17 subfamilies (11). The morphological are only distantly related to other members of Saxifragaceae, diversity encompassed by this group is so great that subse- and (iii) representatives of the Solanaceae (subclass Asteridae) quent workers have provided substantially modified con- appear more closely related to Saxifragaceae (subclass Rosidae) cepts of relationships (9, 12-16). However, these recent than traditionally maintained. These data illustrate the value of schemes often differ dramatically; little agreement exists chloroplast gene sequence data in resolving genetic, and hence regarding the circumscription, taxonomic rank, or relation- phylogenetic, relationships among members of the most taxo- ships of Engler's subfamilies. The differences among taxo- nomically complex groups. nomic treatments are too substantial to review here (see reviews in refs. 10 and 12). We illustrate the magnitude of In many groups of angiosperms phylogenetic relationships at these discrepancies, however, in a simplified comparison of higher taxonomic levels (family and above) have remained relationships (Fig. 1). enigmatic despite detailed morphological analyses. Presum- Most recent workers have considered the Englerian con- ably, these difficulties reflect the more frequent occurrence cept ofSaxifragaceae too broad. Takhtajan (15), for example, of parallel and convergent character state change (ho- distributed the same taxa among more than 10 families and moplasy) at higher taxonomic ranks. Below the familial level, suggested that some members of Saxifragaceae sensu lato restriction site analysis of chloroplast DNA has been excep- were only very distantly related. He placed most families in tionally valuable in resolving phylogenetic affinities (1, 2), two orders (Cunoniales and Saxifragales, superorder Rosa- even when extreme morphological divergence has obscured nae; subclass Rosidae) and considered these to be distantly a close relationship (3). At higher taxonomic levels, however, related to Brexiaceae (Celastrales, superorder Celastranae, restriction site analysis typically is inadequate for phyloge- subclass Rosidae) and Hydrangeaceae (Hydrangeales, super- netic inference, owing to excessive homoplasy and length order Cornanae; subclass Asteridae). His Saxifragaceae are mutation; DNA sequencing appears to be the tool of choice tribe In contrast, in such instances (2, 4, 5). Sequencing of the slowly evolving essentially limited to Engler's Saxifrageae. ribosomal RNA genes, for example, has unequivocally dem- Cronquist (12) placed several of Engler's woody subfamilies onstrated that chloroplasts are of endosymbiotic origin (33). in Grossulariaceae (Fig. 1); he maintained that woody taxa In plants, DNA sequence comparisons of chloroplast- (his Grossulariaceae and Hydrangeaceae) were more usefully encoded genes will be particularly useful in phylogenetic associated with other woody families of Rosidae. Cronquist's analyses at higher taxonomic levels (4, 5). Although few Saxifragaceae encompasses several of Engler's original her- major studies ofchloroplast gene sequences and phylogenetic baceous subfamilies. relationships have been published (6, 7), the chloroplast gene To understand completely the phylogenetic affinities of all rbcL, encoding the large subunit ofribulose-1,5-bisphosphate members of Saxifragaceae sensu lato would require analysis carboxylase, has emerged as the preferred gene for examin- of a large portion of Rosidae, as well as taxa in other ing higher-level phylogenetic relationships (2, 4). The reasons subclasses. Here we concentrate on a suite of taxa that for this preference include (i) rbcL has been widely se- represent well the morphological diversity of the group and ask: can rbcL sequence data elucidate phylogenetic relation- be used to The publication costs of this article were defrayed in part by page charge ships in this enigmatic group? If so, this tool could payment. This article must therefore be hereby marked "advertisement" unravel the evolutionary history ofother equally problematic in accordance with 18 U.S.C. §1734 solely to indicate this fact. groups of plants. 4640 Downloaded by guest on September 25, 2021 Evolution: Soltis et al. Proc. Nati. Acad. Sci. USA 87 (1990) 4641 Takhtajan (1987) Engler (1964) Cronquist (1981) (28), a monocotyledon, distantly related to the other taxa, which are all dicotyledons; Nicotiana otophora (Solanaceae, ROSANAE SAXIFRAGACEAE ROSALES subclass Asteridae) (29); and Pisum sativum (Fabaceae, CUNONIALES subclass Rosidae, but placed in a different order than Saxi- BAUERACEAE Penthoroideae --- , SAXIFRAGACEAE fragaceae) (30). These species served as outgroups in the SAXIFRAGALES // Saxifragoideae parsimony analysis. PENTHORACEAE Ae Vahlioideae , UPGMA dendrograms were calculated from distance ma- SAXIFRAGACEAE Al Francooideae trices based on the 3ST model (31). Maximum-likelihood and VAHUACEAE , / Eremosynoideae parsimony analyses used the DNAML and DNAPARS programs, FRANCOACEAE 0 Lepuropetaloideae respectively, provided in PHYLIP 3.2 (J. Felsenstein); the EREMOSYNACEAE Pamassioideae DNABOOT program (PHYLIP 3.1) was used to obtain confi- LEPUROPETALACEAE Baueroideae * CUNONIACEAE dence levels for the parsimony analysis. For the DNAML PARNASSIACEAE Ribesoideae GROSSULARIACEAE analysis, the transition/transversion ratio was set to 2.0 and GROSSULARIACEAE Pterostemonoideae the empirical frequencies of the bases were used (F option); ITEACEAE * Hydrangeoideae HYDRANGEACEAE runs were conducted with and without Z. mays and the Tetracarpaeoideae CELASTRANAE categories option (C). Because of the length of time needed Iteoideae CELASTRALES to run the program with Z. mays and the C option, these were Escallonioideae not included when the jumble option (J) was used. BREXIACEAEBREXIACEAE ~~Brexioideae CORNANAE Montinioideaegegoideae HYDRANGEALES Phyllonomoideae RESULTS AND DISCUSSION PFEROSTEMONACEAE rbcL in Saxifragaceae sensu lato is 1407 bp long, comparable HYDRANGEACEAE W to the size reported for other taxa (5, 7). Sequences for the TETRACARPACEAE eight taxa analyzed are given in Fig. 2. Due to EcoRI* ESCALLONIACEAE activity, we did not obtain the full length of the rbcL gene MONTINIACEAE from Francoa (our sequence for this taxon begins 471 bp from DULONGIACEAE the 5' end of the gene). Thus, we have sequenced approxi- FIG. 1. Schematic representation of relationships among taxa of mately two-thirds of rbcL from Francoa. Detailed sequence Saxifragaceae sensu lato depicting some of the discrepancies that comparisons (4) indicate, however, that use of a partial gene exist among the traditional (11) and more recent (12, 14) taxonomic sequence (particularly one this large) should not affect phy- treatments. logenetic reconstruction. In fact, we obtained the same results when we used only the last two-thirds ofthe rbcL gene MATERIALS AND METHODS for all taxa in a parsimony analysis. We obtained rbcL sequence data for the following members of A matrix of 3ST
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