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Razafimandimbison Et Al. 2009 Molecular Phylogenetics and Evolution 52 (2009) 879–886 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogenetics and generic assessment in the tribe Morindeae (Rubiaceae–Rubioideae): How to circumscribe Morinda L. to be monophyletic? Sylvain G. Razafimandimbison a,*, Timothy D. McDowell b, David A. Halford c, Birgitta Bremer b a Bergius Foundation, Royal Swedish Academy of Sciences and Botany Department, Stockholm University, SE-10691 Stockholm, Sweden b Department of Biological Sciences, Box 70703, East Tennessee State University, Johnson City, TN 37614, USA c Queensland Herbarium, Environmental Protection Agency, Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Qld 4066, Australia article info abstract Article history: Most of the species of the family Rubiaceae with flowers arranged in head inflorescences are currently Received 13 February 2009 classified in three distantly related tribes, Naucleeae (subfamily Cinchonoideae) and Morindeae and Sch- Revised 14 April 2009 radereae (subfamily Rubioideae). Within Morindeae the type genus Morinda is traditionally and currently Accepted 15 April 2009 circumscribed based on its head inflorescences and syncarpous fruits (syncarps). These characters are Available online 24 April 2009 also present in some members of its allied genera, raising doubts about the monophyly of Morinda. We perform Bayesian phylogenetic analyses using combined nrETS/nrITS/trnT-F data for 67 Morindeae Keywords: taxa and five outgroups from the closely related tribes Mitchelleae and Gaertnereae to rigorously test Appunia the monophyly of Morinda as currently delimited and assess the phylogenetic value of head inflores- Coelospermum Gynochthodes cences and syncarps in Morinda and Morindeae and to evaluate generic relationships and limits in Mor- Head inflorescences indeae. Our analyses demonstrate that head inflorescences and syncarps in Morinda and Morindeae are nrETS evolutionarily labile. Morinda is highly paraphyletic, unless the genera Coelospermum, Gynochthodes, nrITS Pogonolobus, and Sarcopygme are also included. Morindeae comprises four well-supported and morpho- Paraphyly logically distinct major lineages: Appunia clade, Morinda clade (including Sarcopygme and the lectotype Phylogenetic classification M. royoc), Coelospermum clade (containing Pogonolobus and Morinda reticulata), and Gynochthodes–Mor- Rubiaceae inda clade. Four possible alternatives for revising generic boundaries are presented to establish monophy- Syncarps letic units. We favor the recognition of the four major lineages of Morindeae as separate genera, because trnT-F this classification reflects the occurrence of a considerable morphological diversity in the tribe and the phylogenetic and taxonomic distinctness of its newly delimited genera. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction Petit), Lasiantheae B. Bremer & Manen (Lasianthus Jack), Mitchel- leae Razafim. & B. Bremer (Damnacanthus C.F. Gaertn. and Mitchella A recent molecular phylogenetic study of Razafimandimbison L.), and Prismatomerideae Ruan (Prismatomeris Thw. and its allied et al. (2008) based on five plastid gene and nrITS regions led to genera). The Samoan genus Sarcopygme Setch. & Christoph., classi- the establishment of new tribal limits for the species-rich Psychot- fied by Darwin (1979) in Morindeae, was excluded from Morindeae rieae alliance of the subfamily Rubioideae (Rubiaceae or coffee sensu Razafimandimbison et al. (2008) (hereafter called Morin- family). These authors recircumscribed the tribe Morindeae in a deae) mainly because of its numerous (up to 100) and synchronous narrow sense to include only six genera (Appunia Hook.f., Coelo- flowers with uniovulate locules. spermum Blume, Gynochthodes Blume, Morinda L., Pogonolobus F. Morindeae is a pantropical group of ca. 160 species assigned to Muell., and Siphonandrium K. Schum.). The members of Morindeae six genera whose generic limits are controversial and remain can be diagnosed by the following features: massive T-shaped pla- unsettled. Of these genera, the most species-rich genus is Morinda, centae inserted in the middle of the septum with two anatropous one of the 24 rubiaceous genera that Linnaeus described in his vol- ovules per carpel and pyrenes with a single lateral germination slit ume Species Plantarum (Linnaeus, 1753). Linnaeus (1753) included (Igersheim and Robbrecht, 1993). Some genera traditionally associ- three species (M. citrifolia L., M. royoc L., and M. umbellata L.) in his ated with Morindeae are currently classified in the following genus Morinda, which can be characterized by a combination of its tribes: Colletoecemateae Rydin & B. Bremer (Colletoecema E.M.A head inflorescences and syncarpous fruits (=syncarps or multiple fruits with ovaries fused). Head inflorescences (also known as capitula, Johansson, 1994)inMorinda sensu Linnaeus (1753) * Corresponding author. Fax: +46 (0)8 165525. E-mail address: sylvain.razafi[email protected] (S.G. Razafimandim- consist of two to many flowers clustered together on a common bison). receptacle. These heads are either solitary (i.e., one cluster of 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.04.007 880 S.G. Razafimandimbison et al. / Molecular Phylogenetics and Evolution 52 (2009) 879–886 flowers on a peduncle = single head) or umbel-like; the later are material for all investigated taxa, except Sarcopygme pacifica and unbranched and comprised of two to many heads. Within each isolated following the mini-prep procedure of Saghai-Maroof capitulum the number of flowers varies from 2 to 50 but is fairly et al. (1984), as modified by Doyle and Doyle (1987). For S. pacifica constant within species. Steyermark (1972) merged the neotropi- total DNA was extracted from a dry young inflorescence (Tronquet cal Morindeae genus Appunia bearing head inflorescences/infruct- 749, P!). Isolated DNA was amplified and sequenced according to escences composed of free flowers/fruits in Morinda. This the protocols outlined in the following articles: Razafimandimbi- taxonomic decision broadened the morphological concept of Mor- son et al. (2005) for nrETS, Razafimandimbison and Bremer inda and resulted in disagreements among Rubiaceae specialists (2002) for trnT-F, and Razafimandimbison and Bremer (2001) and over its circumscription. For example, Hayden and Dwyer (1969), Razafimandimbison et al. (2004) for nrITS. The primers from these Johansson (1987), Burger and Taylor (1993), and Lorence (1999) previous studies were used for the nrETS, nrITS, and trnT-F regions. retained Appunia at generic level, while Andersson (1992), Boom In all PCRs, one reaction was run using water instead of DNA as a and Delprete (2002), and Taylor and Steyermark (2004) included negative control to check for contamination. All sequencing reac- Appunia in Morinda. The occurrence of head inflorescences and syn- tions were performed using the Big DyeÒ Terminator v3.1 Cycle carpous fruits in some members of its allied genera of Morinda Sequencing kit and Big DyeÒ Terminator v1.1 Cycle Sequencing (Coelospermum and Gynochthodes) raises doubts regarding the kit (Applied Biosystems) and sequences were analyzed with the monophyly of the genus. Morinda currently comprises ca. 130 spe- 3100 Genetic Analyzer (Applied Biosystems). cies of lianescent, arborescent, and suffrutescent plants whose phylogenetic affinities with the other Morindeae genera have 2.3. Phylogenetic analyses never been assessed. The main objective of this study is to reconstruct a robust phy- Sequence fragments were assembled using the Staden package logeny of the tribe Morindeae using combined plastid (trnT-F) and (Staden, 1996). All new sequences have been submitted to nuclear (nrETS and nrITS) DNA sequence data. The resulting phy- GenBank (FJ906973–FJ907161, Table 1). For each DNA sequence logeny will be used to: (1) rigorously test the monophyly of Morin- region (or marker) all new sequences and published ones taken da as presently delimited; (2) evaluate the phylogenetic value of from GenBank were aligned together using the computer program head inflorescences and syncarps traditionally and currently used CLUSTAL-X (Thompson et al., 1997) to produce an initial alignment for circumscribing genera in Morinda and Morindeae; (3) and as- and manually adjusted using software SeAl v.2.0 (Rambaut, 1996). sess the current generic relationships and limits in Morindeae. Insertion/deletion events were inferred by eye and gaps were treated as missing data in the alignments. The aligned matrices were analyzed with Bayesian inference without coded indels. 2. Materials and methods Separate and combined Bayesian analyses of sequence data were performed in MrBayes 3.1.2 (Huelsenbeck and Ronquist, 2.1. Taxon sampling 2001; Ronquist and Huelsenbeck, 2003). For each of the three DNA sets, the best performing nucleotide substitution model was We investigated a total of 67 taxa of Morindeae, including Mor- selected using the computer programs MrModeltest 2.0 (Nylander, inda (ca. 41 species), the neotropical genus Appunia (six species), 2001) and MrAIC ver. 1.4.3 (Nylander, 2004). The best performing the Australasian genera Coelospermum (six species) and Gynochth- evolutionary models were estimated under three different model odes (four species) and the monotypic New Guinean and northern selection criteria: Akaike information criterion (AIC) (Akaike, Australian genus Pogonolobus (one individual). We were unable to
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