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Phylogenetic Relationships and Floral Evolution in the Papilionoid Legume

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Phylogenetic Relationships and Floral Evolution in the Papilionoid Legume Phylogenetic relationships and ¯oral evolution in the papilionoid legume clade Amorpheae MICHELLE M. MCMAHON McMahon, M. M. (University of California, Davis, One Shields Avenue, Davis, CA, 95616, U.S.A.; e-mail: [email protected]). Phylogenetic relation- ships and ¯oral evolution in the papilionoid legume clade Amorpheae. Brittonia 57: 397±411. 2005.ÐAmorpheae (Fabaceae: Papilionoideae) was ®rst considered a natural group by Rupert Barneby in his illustrated monograph Daleae Imagines. Amorpheae currently comprise eight genera, ca. 250 spp., and extensive ¯oral diversity, including loss of corolla and addition of a stemonozone. The Amor- pheae and many of Barneby's subtribal groups are supported as monophyletic by previous phylogenetic analysis of nuclear ribosomal and chloroplast sequence data. However, some relationships remain unclear. A nuclear marker derived from a genomic study in Medicago, CNGC4, was sequenced in selected Amorpheae. This is one of the ®rst applications of this marker for phylogenetic study. The new data con®rm some relationships inferred using trnK and ITS, but also provide evidence for new arrangements. Combined data were used to explore several aspects of Barneby's taxonomic framework. The phylogeny, in concert with data on ¯oral morphology, implies that simpli®cation of the complex papilionoid ¯ow- er has occurred several times in the history of the Amorpheae. Key words: Amorpheae, Barneby, CNGC4, Dalea, ¯oral evolution, Papiliono- ideae. Amorpheae Borrissova emend. Barneby was conducted, Barneby presented a hy- is a group of ca. 250 papilionoid legume pothesis of relationships among groups in species with much variation in ¯oral form. Amorpheae (Fig. 2). This hypothesis was Although nested within the Papilionoideae based on several informative morphological (Lavin et al., 2001; McMahon & Hufford, characters, some of which are consistent 2004; Wojciechowski et al., 2004) the with the phylogeny based on DNA se- group contains many members with ¯owers quences, some of which are not. that depart from the standard papilionoid Previous analyses resulted in very strong form. Aspects that vary include a unique support for a clade of three genera (the dal- structure (the ``stemonozone'', Fig. 1A, B; eoids: Dalea, Marina, Psorothamnus), sis- McMahon & Hufford, 2002), losses of ter to a clade of the remaining ®ve genera structures such as petals and stamens, and (the amorphoids: Errazurizia, Parryella, the loss of petal attributes such as asym- Eysenhardtia, Amorpha, and Apoplanesia) metry and strong blade/claw distinctions (McMahon & Hufford, 2004). Furthermore, (Fig. 1C, D; McMahon & Hufford, 2005). relationships among many lineages within First considered a natural group by Rupert the daleoids were strongly supported. How- Barneby (1977), Amorpheae is natively dis- ever, within the amorphoids, the previously tributed from southern Canada to northern used markers (ITS and the trnK intron) var- Chile, with areas of highest diversity in the ied little. These taxa are particularly inter- arid and semi-arid regions of Mexico, the esting because they include several appar- Andes, and the prairies of North America. ent simpli®cations from the complex papi- Although no explicit phylogenetic analysis lionoid ¯ower. Therefore, additional data Brittonia, 57(4), 2005, pp. 397±411. ISSUED: 28 December 2005 q 2005, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 398BRITTONIA [VOL. 57 FIG.1. Selected aspects of variation among ¯owers of Amorpheae. A. Schematic of a generalized member of Marina or Dalea showing the lateral petals attaching above the hypanthium (asterisks). The region between the petal insertion and the hypanthium is the stemonozone (McMahon & Hufford, 2002). B. Scanning electron micrograph of Dalea pulchra Gentry; proximal portion of bud near anthesis (calyx mostly removed), showing lateral petal attachment points. C. Line drawing of lateral petals, Psorothamnus scoparius (A. Gray) Rydb., showing difference between wing and keel, asymmetry within each petal, and distinction between claw (narrow proximal region) and blade (distal laminate region). D. Line drawing of lateral petals, Errazurizia megacarpa (S. Wats.) I. M. Johnst., showing similarity of wing to keel, near symmetry within petals, and gradual tapering of distal region to proximal region. [In all, distal is up and adaxial (with respect to the in¯orescence axis) is to the left. b, banner petal; c, calyx; g, gynoecium; h, hypanthium (arrow points to rim); k: keel petal; st, stamens; w: wing petal. Scale bar (B) 5 0.5 mm.] are required, ideally from a region that is independent from the ribosomal and chlo- roplast sequences used previously. Markers derived from genomic data in Medicago truncatula have been recently developed for comparative genome studies across crop le- gumes (Choi et al., 2004b). Application of these markers to phylogenetic questions is promising but not always straightforward (Scherson et al., 2005). Extending their ap- plication from Medicago to a group such as FIG.2. Evolutionary relationships among mem- Amorpheae, diverged for perhaps tens of bers of Amorpheae as previously hypothesized, from millions of years (Choi et al., 2004b), may Barneby's Figure 1 (Barneby, 1977: 13). help provide resolution within Amorpheae. 2005] McMAHON: PHYLOGENETICS & FLORAL EVOLUTION OF AMORPHEAE 399 TABLE I GENBANK ACCESSION NUMBERS FOR NEWLY GENERATED AND DOWNLOADED SEQUENCES GenBank Taxon Collection accession Sequences submitted: CNGC4 Amorpha apiculata Wiggins Fishbein 3745 (ARIZ) DQ023320 Amorpha californica Nutt. ex Torr. & A. Gray Grable 6434 (WS) DQ023322 Amorpha canescens Pursh McMahon 683 (WS) DQ023323 Apoplanesia paniculata C. Presl Cabrera C. 5479 (ARIZ) DQ023327 Errazurizia benthami (Brandegee) I. M. Johnst. McMahon 438 (WS) DQ023324 Errazurizia megacarpa (S. Watson) I. M. Johnst. Fishbein 3773 (WS) DQ023321 Errazurizia rotundata (Wooton) Barneby McMahon 452 (WS) DQ023325 Eysenhardtia orthocarpa (A. Gray) S. Watson Fishbein 3683 (ARIZ) DQ023328 Eysenhardtia texana Scheele Van Devender 29V79 (ARIZ) DQ023326 Parryella ®lifolia Torr. & A. Gray ex A. Gray Porter 8868 (ARIZ) DQ023329 Psorothamnus fremontii (Torr. & A. Gray) Barneby McMahon 339 (ARIZ) DQ023330 Psorothamnus kingii (S. Watson) Barneby McMahon 688 (ARIZ) DQ023331 Psorothamnus schottii (Torr.) Barneby McMahon 150 (ARIZ) DQ023332 GenBank Taxon Sequence region accession Sequences downloaded Amorpha fruticosa ITS AFU59890 Amorpha fruticosa matK AF270861 Apoplanesia paniculata ITS AF187093 Apoplanesia paniculata matK AF270860 Dalea pulchra matK AY386860 Eysenhardtia orthocarpa matK AY386909 Eysenhardtia sp. Lavin 5052 ITS AF187096 Marina parryi matK AY386859 Marina sp. Lavin 5341 ITS AF187095 Medicago truncatula CNGC4 BV164997 Medicago truncatula ITS AF233339 Medicago truncatula matK AF522109 Pisum sativum CNGC4 BV165002 Pisum sativum ITS AY143481 Pisum sativum matK AY386961 For all other accession numbers, see McMahon and Hufford (2004). It will also be of value in exploring the ben- la as CNGC4 (cyclic nucleotide-regulated e®ts of transferring data from comparative ion channel like protein) (Choi et al., genomic analyses to phylogenetic system- 2004a) was sequenced for 13 Amorpheae atics. (Table I). Although many markers will be The goals of this paper are (1) to present examined in the future, this marker was se- a preliminary set of data from one genomic lected to be ®rst based on its potential for derived nuclear marker, CNGC4, alone and variation among species (Choi et al., 2004b; in combination with previously reported Scherson et al., 2005). Additionally, the DNA sequence data, (2) to summarize cur- primers uniformly produced a single PCR rent understanding of Amorpheae relation- band and a clean sequencing chromato- ships, (3) to review patterns of ¯oral evo- gram, consistent with the possibility that the lution in Amorpheae, and (4) to compare region is single-copy in Amorpheae, al- these inferences to Barneby's hypotheses of though this is not yet con®rmed. Taxa were ¯oral evolution in the group. chosen based on their placement in previ- ous phylogenetic analyses, in which many Methods and Materials relationships were resolved with strong sup- The nuclear region identi®ed in the ge- port. However, relationships among key nome-wide analysis of Medicago truncatu- taxa that are involved in ¯oral simpli®ca- 400BRITTONIA [VOL. 57 tions were not well resolved (McMahon & the trees obtained. No strongly supported Hufford, 2004, 2005). Therefore, available relationships ($ 90% bootstrap; Felsen- members of Eysenhardtia, Errazurizia, stein, 1985) differed among the trees. Ad- Amorpha, Parryella, and Apoplanesia (the ditionally, the partition homogeneity test (or amorphoid clade) were selected for se- incongruence length difference test, Farris quencing CNGC4. Three members of Pso- et al., 1994) as implemented in PAUP* rothamnus were chosen to span the root of (Swofford, 2003) with 1000 replicates, the daleoid clade (Graybeal, 1998; McMa- failed to reject homogeneity (P 5 0.8220). hon & Hufford, 2004) in an effort to resolve This method may be inappropriate as a test the position of the amorphoid root. Se- for combinability (Barker & Lutzoni, quences from Medicago truncatula and Pis- 2002), but the negative result, in concert um sativum were obtained from GenBank with the lack of strong con¯icting signal, (Table I) and included as outgroups. Addi- provides justi®cation for combining the tional ITS and trnK sequences from Amor- data. pheae have been submitted
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