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Phylogenetics of Seed Plants: an Analysis of Nucleotide Sequences from the Plastid Gene Rbcl James F

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Phylogenetics of Seed Plants: an Analysis of Nucleotide Sequences from the Plastid Gene Rbcl James F Boise State University ScholarWorks Biology Faculty Publications and Presentations Department of Biological Sciences 1-1-1993 Phylogenetics of Seed Plants: An Analysis of Nucleotide Sequences from the Plastid Gene rbcL James F. Smith Boise State University This document was originally published by Biodiversity Heritage Library in Annals of the Missouri Botanical Garden. Copyright restrictions may apply. Image courtesy of Biodiversity Heritage Library. http://biodiversitylibrary.org/page/553016 See article for full list of authors. PHYLOGENETICS OF SEED Mark TV Chase,' Douglas E. Soltis,' PLANTS: AN ANALYSIS OF R ichard C. Olmstead;' David Morgan,J Donald H Les,' Brent D. Mishler," NUCLEOTIDE SEQUENCES Melvin H, Duvall,' Hobert A. Price,' FROM THE PLASTID Harold G. Hills,' Yin· Long Qiu,' Kathleen A. Kron,' Jeffrey H. Hell.ig,' GENE rb ell Elena Cont.':, 10 Jeffrey D. Palmer, 1l James R. ft1an/wrt,9 Kenneth}. Sylsma, 1O Helen J . Michaels," W. John Kress, " Kenneth C. Karol, 1O W. Dennis Clark, 13 lvlikael J-I edren,u Brandon S. Gaut,? Robert K. J ansen, l ~ Ki.Joong Kim ,'5 Charles F. Jf/impee,5 James F. Smilh,I2 Glenn N. Furnier,lo Steven 1-1. Strauss,l? Qiu- Yun Xian g,3 Gregory 1.1. Plunkeu,J Pamela S. Soltis ,:" Susan M. Swensen, ]!J Stephen /, ', Williams," Paul A. Gadek,'" Christopher }. Quinn,20 Luis E. /:.guiarle,7 Edward Golenberg," Gerald 1-1. Learn, jr.,7 Sean W. Graharn,22 Spencer C. H. Barreu," Selvadurai Dayanandan,23 and Victor A. Albert' AIJSTRACf We present the results of two exploratory parsimony analyses of DNA sequences from 475 and 499 species of seed plants. respectively. representing all major taxonomic groups. The data are exclusively from the chloroplast gene rbeL. which codes for the large subunit of ribulose-l .5-bisphosphate carboxylase/ oxygenase (RuBisCO or RuBPCase). We used two different state-transformation assumptions resulting in two sets of cladograms: (i) equal.weight ing for the 499-taxon analysis: and (ii) a procedure that differentially weights transversions over transitions within characters and codon positions among characters for the 475·taxon analysis. The degree of congruence between these results and other molecular. as well as morphological, cladistic studies indicates that rbc L sequence va riation contains historical evidence appropriate for ph yloge netic analysis at this taxonomic level of sampling . Because the topologies presented are necessarily approximate and cannot be evaluated adequately for in ternal support, these results should be assessed from the perspective of their predictive value and used to direct future studies. both molecular and morphological. In both analyses. the three genera of Gnetales are placed together as the sister group of the no ..... ering plants. and the anomalous aquatic Ce ratoph),lIllm (Ceratophyll aceae) is sister to all other flo ..... ering plants. Several major lineages identified correspond well with at least some recent taxonomic schemes fo r angiosperms. particularly those of Dahlgren and Thorne. The basalmost clades within the angiosperms are orders of the apparentl y polyphyletic subclass Magnoliidae sensu Cronquist. The most conspicuous feature of the topology is that the major di vision is not monoco! versus di cot. but rather one correlated with general pollen type: uniaperturate versus triaperturate. The Dilleniidae and Humamelidae are the only subclasses that are grossly polyphyletic; an examination of the la tter is presented as an example of the use of these broad analyses to focus more restricted slUdies. A broadly circumscribed Rosidae is para phyletic to Asteridae and Dilleniidae. Subclass Caryophyllidae is monophyletic and derived frolll within Rosidae in the 475-taxon analysis but is sister to a group composed of broadly delineated Asteridae aud Rosidae in the 499-taxon study. , The authors acknowledge the following support: U.S. National Science Foundation (NSF) grant BSR-8906496 to MWC; 8SR·9007614 to DES; BSR·900232I to MRD; 8SR·9107827 to RGO; 8SR·881 7992 to DHL "nd CFW; BSR·9107484 to 8DM; BSR·9007293 and BSR·9020055 to KJS; 8SR·882 1264 to KAK; 8SR·8717600 "nd 8SR . 8996262 to lOP; 8SR·9020171 to RKJ ; BSR·8817953 to SHS "nd RAP and BSR·8957023 to SHS; BSR·880193 to W. Alverson; a Sloan Postdoctoral Fellowship to KJK: BSR-89l4635 to VAA; a grant fr om the American Philosophical Society to SEW; Australian Research Council grant AD903 185 1 to PAG and CJQ: an operating grant to SCHB and a graduate scholarship to SWG from the Natura l Sciences & Engineering Research Council of Canada; a grant to MWC and doctoral fellowship to VAA fr om the American Orchid Society; and a postdoctoral scholarship ANN. MISSOURI BOT. CARD. 80: 528- 580. 1993. Volume 80, Number 3 Chase et al. 529 1993 Phylogenetics of Seed Plants Curre nt assessments of hi ghe r-level relationships taxa fr om 135 families, slill less than a thi rd of in seed pla nts a re based largely on informed judg­ angiosperm families. I f insuffi cient sampling of taxa ments of the relati ve value of variolls reproductive or characters (i.e., sequence length, acknowledged a nd vegeta tive characters (including secondary as a problem with the rbcS data studied by Martin chemistry) and to some exte nt on historical pre­ & Dowd, 1991) are indeed fa ctors, then no valid cedent. Authors of recent taxonomic schemes (for investigation of the "informativeness" of a given example. Dahlgren. 1980; T ak hlajan. 1980, 1987, gene sequence exists for seed plants. Thus we are Cronquist, 198 1 ~ Thorne, 1983, 1992) ha ve syn­ le ft wi th only an unfounded assessment of sequence thesized an enormous a mou nt of information. Ne v. data as having the potential to aid in estimating ertheless, their taxonomic decisions have been guid­ higher. level relationships. ed by estimations of whic h characters a re reliable Suggestions that the chloroplast gene rbcL, whi ch indica tors of relationships. These diffe ring judg­ codes for the la rge subunit of ribulose· I ,5-bis­ ments are responsible for radical differences in phosphate carboxylase/ oxygenase (RuBisCO or delimitation and relative ra nks of taxa in each RuBPCase), was an appropriate locus to use in system of classification. Recently, a number of phylogenetic studies began with Ritland & Clegg explicit, cladistic hypotheses have been developed (1987) a nd Zurawsk; & Clegg (1987). In;l;al al· at inclusive hie rarchi cal levels (e.g., Crane, 1985, tempts to evaluate relationships used only a doze n 1988; Dahlgren & Bremer, 1985; Dahl gren ct al. , or so sequences representin g a ll land plants (Palm er 1985, Doyle & Donoghue, 1986. 1992, Bremer et a I. , 1988; Ciannasi et al. , 1992). Other rcccnt et aI., 1987; Donoghue & Doyle, 1989; Loconte studies have been restricted to single families (Doc­ & Stevenson, 1991; Martin & Dowd, 1991; Ham­ bley et al., 1990; Kim et aI., 1992) or putatively by & Zimmer, 1992; Hufford , 1992; Olmstead et closely related families (Soltis et aI., 1990; Les et al.. 1992, Taylor & H; ckey. 1992). Such clad;sl;c aI. , 1991; Donoghue et a I. , 1992; Olmstead et al. studies have previously been limited in scope; some 1992, Rett;g el a I. , 1992). Mosl of Ih e la ttce data matrices contain significant taxonomic gaps, studies began the process of incorporating signifi ­ and in others characters for some taxa are missing. cantl y greater sampling to enhance their phylo­ Both of these fa ctors may have unpredictably mis­ genetic perspec ti ve. The use of rbcL was spurrcJ leading effects (Nixon & Davis, 199 1; Plat nick et by C. Zurawski, wh o generously made avai lable a aI., 1991). Despite a great deal of investigation set of internal sequencing primers. The advent of and analysis, seed.plant phylogenetics is, at best, temperature cyclers and hi gh.temperature- resis. in a prelimina ry stage of in vestigation and knowl­ tant DNA polymerases (sometimes terme<\ Poly. edge. merase Chain Reaction or PCR) has greatly en­ Molecular data, spec ifi cally DNA sequences, hanced rates at wh ich gene sequence data a rc ha ve received a great deal of attent ion as a potential accumulating, so that effects on phylogenetic es­ source of "phylogenelically informative" cha rac­ timates of more intensive sampling of sequence ters Iha t are putatively less ambiguous than non· variation can now be investigated. molecular characters. Such pronouncements suffer We wish to examine here the degree to whi ch from the limitation that, at higher taxonomic levels, a representative sa mpling of sequence variation for no extensive sampling and phylogenetic description rbc L contains evidence of the evolutionary history of DNA sequence variation has taken place. The of seed plants. In this stud y, we address the <Iualit y most taxonomically comprehensive a nal ysis of nu· of evidence present in rbr L sequences for all major cleic acid sequences published so far on plants seed·plant lineages (roughl y 265 families, the exact (rH NA; Hamby & Zim mer, 1992) used onl y 60 number depending on the taxonomic scheme fol· taxa, and a number of these were partial sequences. lowed). To a limited extent, we wi ll compare our Martin & Dowd ( 199 1), using nucleic acid se­ phylogenetic hypotheses with recent schemes, but quences of the small subunit of RuBisCO (rbcS) such comparisons are diffi cult and must be consid­ inferred from amino acid sequences, studied 335 ered heuristic because sister-group relationships ex- from the OGAPA. Univcrsidad Nacional Autonoma de Mexico. Mexico. to LEE. We also thank David L. Swofford and John M. Mercer fo r assistance and advice in running the parsimony analyses; William S. Alverson. Michael T. Clegg. Juli e Dowd . E. Allcn Hcrre. Peter G. Martin. and James E. Rodman. for access to their unpublished sequences; Jeffrey 1.
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