Evolutionary Relationships in the Asteraceae Tribe Inuleae (Incl

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Evolutionary Relationships in the Asteraceae Tribe Inuleae (Incl ARTICLE IN PRESS Organisms, Diversity & Evolution 5 (2005) 135–146 www.elsevier.de/ode Evolutionary relationships in the Asteraceae tribe Inuleae (incl. Plucheeae) evidenced by DNA sequences of ndhF; with notes on the systematic positions of some aberrant genera Arne A. Anderberga,Ã, Pia Eldena¨ sb, Randall J. Bayerc, Markus Englundd aDepartment of Phanerogamic Botany, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden bLaboratory for Molecular Systematics, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden cAustralian National Herbarium, Centre for Plant Biodiversity Research, GPO Box 1600 Canberra ACT 2601, Australia dDepartment of Systematic Botany, University of Stockholm, SE-106 91 Stockholm, Sweden Received27 August 2004; accepted24 October 2004 Abstract The phylogenetic relationships between the tribes Inuleae sensu stricto andPlucheeae are investigatedby analysis of sequence data from the cpDNA gene ndhF. The delimitation between the two tribes is elucidated, and the systematic positions of a number of genera associatedwith these groups, i.e. genera with either aberrant morphological characters or a debated systematic position, are clarified. Together, the Inuleae and Plucheeae form a monophyletic group in which the majority of genera of Inuleae s.str. form one clade, and all the taxa from the Plucheeae together with the genera Antiphiona, Calostephane, Geigeria, Ondetia, Pechuel-loeschea, Pegolettia,andIphionopsis from Inuleae s.str. form another. Members of the Plucheeae are nestedwith genera of the Inuleae s.str., andsupport for the Plucheeae clade is weak. Consequently, the latter cannot be maintained and the two groups are treated as one tribe, Inuleae, with the two subtribes Inulinae andPlucheinae. The genera Asteriscus, Chrysophthalmum, Inula, Laggera, Pentanema, Pluchea, and Pulicaria are demonstrated to be non-monophyletic. Cratystylis and Iphionopsis are foundto belong to the same clade as the taxa of the former Plucheeae. Caesulia is shown to be a close relative of Duhaldea and Blumea of the Inuleae-Inulinae. The genera Callilepis and Zoutpansbergia belong to the major clade of the family that includes the tribes Heliantheae sensu lato andInuleae (incl. Plucheeae), but their exact position remains unresolved.The genus Gymnarrhena is not part of the Inuleae, but is either part of the unresolvedbasal complex of the paraphyletic Cichorioideae, or sister to the entire Asteroideae. r 2005 Gesellschaft fu¨ r Biologische Systematik. Publishedby Elsevier Gmbh. All rights reserved. Keywords: Asteraceae; Inuleae; Inulinae; Plucheinae; Phylogeny; ndhF Introduction papers (Bremer, 1987; Anderberg, 1989; Karis et al., 1992; Kim andJansen, 1995 ; Eldena¨ s et al., 1999; The subdivision of the former tribe Inuleae into three Panero andFunk, 2002 ). The separation of tribe smaller groups has gainedsupport in a number of Gnaphalieae from the rest of the Inuleae complex is well supported and evidently correct, but the delimita- ÃCorresponding author. tion of the other genera of the Inuleae, referredto as E-mail address: [email protected] (A.A. Anderberg). tribes Inuleae s.str. andPlucheeae by Anderberg (1989, 1439-6092/$ - see front matter r 2005 Gesellschaft fu¨ r Biologische Systematik. Publishedby Elsevier Gmbh. All rights reserved. doi:10.1016/j.ode.2004.10.015 ARTICLE IN PRESS 136 A.A. Anderberg et al. / Organisms, Diversity & Evolution 5 (2005) 135–146 1991a, b), have not been fully understood. Early group with other taxa of Gnaphalieae, with Inuleae analyses of molecular data based on ndhF sequence s.str., or with the Plucheeae. The genus Pelucha, which data (Kim andJansen, 1995 ; Eldena¨ s et al., 1999) with great hesitation was acceptedin the Plucheeae by showedthat the Inuleae andPlucheeae are sister groups, Anderberg (1994), has been foundto belong in the andthat they together constitute the sister group of Heliantheae (Baldwin and Wessa, 2000), andwas not Heliantheae s. lat., Eupatorieae, andthe African investigatedfurther by us. Anisopappus, Athroisma and Blepharispermum, three genera formerly included in the Inuleae (Merxmu¨ ller et al., 1977). Only three genera from Inuleae s.str. andPlucheeae Material and methods were included in the study by Kim andJansen (1995) , andthis small sample size didnotallow for any Molecular methods statements on whether the two representedmonophy- letic groups, or one was derived within the other. To DNA was extractedfrom leaves taken from herbar- clarify this issue, Eldena¨ s et al. (1999) investigatedthe ium specimens or from material dried in silica gel. relationships between the two tribes with a larger sample Voucher information for new ndhF sequences is of taxa. They showedthat the tribe Plucheeae formed presentedin the AppendixA, other sequences are those one clade and that the majority of taxa from the Inuleae usedby Eldena¨ s et al. (1999), or more recent depositions s.str., as circumscribedby Anderberg (1989, 1991a), in GenBank (Asteriscus spp., Pallenis spp., Schizogyne, formedanother. However, their studyfailedto resolve Vierea, Xerolekia). For many extractions, leaves were the positions of three genera from the Inuleae s.str., i.e. groundin liquidnitrogen with mortar andpestle, and Antiphiona, Geigeria, and Pegolettia, in relation to the DNA subsequently extractedwith the methodof Plucheeae andInuleae clades,andthus left tribal Saghai-Maroof et al. (1984) as modified by Doyle and delimitation somewhat unclear. In the same paper, Doyle (1987). For others, leaves were groundwith a Eldena¨ s et al. (1999) described the presence of a Mini-BeadBeater (BioSpec Products,Bartlesville, Ok- characteristic 3-bp insertion in ndhF (CCT in position lahoma, USA) andsubsequently treatedwith the 1588 from 50 endof the Inula sequence in GenBank DNEasy plant DNA extraction kit from Qiagen (Qiagen Accession No. L39453) as characteristic of taxa belong- Inc., Valencia, California, USA), following the manu- ing to the Inuleae s.str. clade. The same genera that were facturer’s protocol. All PCR reactions were performed shown to have this 3-bp insertion are also characterized with 10 mmol/l primers in 25-ml reactions using ‘‘Ready- by a large, rhomboidoxalate crystal in each cell of the to-go’’ PCR beads from Pharmacia Biotech (Amersham cypsela epidermis (Anderberg 1989, 1991a). The 3-bp Pharmacia Biotech, Uppsala, Sweden), following the insertion is absent from all other Asteraceae, including manufacturer’s standard protocol and generally with the all the genera of the Plucheeae clade, and notably also thermal cycling profile, 95 1C for 5 min, followedby 45 from the three genera of unclear systematic position or 55 cycles of 95 1C for 30 s, 45 1C30s,721C 2 min, and mentionedabove ( Antiphiona, Geigeria, and Pegolettia). finally 72 1C for 8 min. Primers usedare those of Eldena¨ s Our present investigation includes a still larger sample et al. (1999). of taxa, aiming at a better understanding of the For sequencing reactions in some taxa, the Thermo relationships between Inuleae andPlucheeae in order Sequenase Fluorescent Sequencing Kit from Pharmacia to resolve their tribal status. Apart from elucidating (Amersham Pharmacia Biotech AB, Uppsala, Sweden) tribal interrelationships, we have also triedto shedlight was used. Fragments were sequenced using fluorescently on the issue of monophyly of some of the larger genera, labeled(CY-5) primers. Fragments were separatedon an such as Blumea, Pluchea, Inula, and Pulicaria,by ALF-Express (Pharmacia Biotech AB, Uppsala, Swe- including several representatives of each in the analysis. den). For most taxa the ‘‘Big Dye Terminator Sequen- Furthermore, we have included a number of genera cing’’ kit (AppliedBiosystems, Warrington, Cheshire, whose systematic positions have been debated, or which UK) was used, and fragments were separated on an have an aberrant morphology comparedto typical ABI377 from AppliedBiosystems. Primers usedfor members of these tribes. Such genera are Caesulia, PCR andfor sequencing are the same as those usedby Callilepis, Cratystylis, Gymnarrhena, Iphionopsis, Rho- Eldena¨ s et al. (1999). Sequences were assembledwith the dogeron, Sachsia, Zoutpansbergia, andalso Dielitzia. Staden software (Staden et al., 1998), andalignedwith The latter was described as a member of Inuleae, but the BioEdit software (Hall, 1999). Two sequences, was included in the Gnaphalieae by Anderberg (1991c). unpublishedat the time of our analysis, from Rhodoger- Like Dielitzia, many Australian Gnaphalieae have more on coronopifolius (GenBank Acc. No. AY226799)and or less cartilaginous bracts without the papery lamina from Sachsia polycephala (AY226800), were kindly that is typical of most representatives of that tribe, andit provided by Javier Francisco-Ortega, Florida Interna- was of interest to test if a taxon such as Dielitzia would tional University. All 63 new ndhF sequences have been ARTICLE IN PRESS A.A. Anderberg et al. / Organisms, Diversity & Evolution 5 (2005) 135–146 137 submittedto GenBank (Accession Nos. AY780811– Boopis Barnadesia Dasyphyllum AY780873; see Appendix A). 95 100 Chuquiraga 98 Doniophyton 78 Schlechtendahlia Phylogenetic analyses Mutisia Adenocaulon Gochnatia The alignment of ndhF sequences resultedin a data Onoseris Stifftia matrix with 184 taxa and2280 characters of which 660 Leibnitzia Gerbera 100 were informative for phylogenetic analysis. The data 93 Piloselloides was analyzedwith parsimony jackknifing ( Farris et al., Nassauvia 100 Trixis 1996), using the computer
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