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Botanical Journal of the Linnean Society, 2013, 173, 387–406. With 2 ﬁgures
Phylogenetic relationships and new tribal delimitations in subfamily Ixoroideae (Rubiaceae)
KENT KAINULAINEN1,2*, SYLVAIN G. RAZAFIMANDIMBISON1,2 and BIRGITTA BREMER1,2
Bergius Foundation, The Royal Swedish Academy of Sciences, SE-106 91 Stockholm, Sweden Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden
Received 4 April 2012; revised 2 October 2012; accepted for publication 31 January 2013
Subfamily Ixoroideae is one of three major lineages in Rubiaceae, with approximately 4000 species. Previous molecular phylogenetic studies have indicated that many genera and tribes previously placed in other subfamilies are better considered as part of Ixoroideae. However, the internal resolution and clade support have generally been low, and several genera found to be nested in the subfamily do not appear to be associated with any described tribe. In order to resolve the phylogeny and assess the tribal delimitations in the expanded Ixoroideae, phylogenetic reconstructions were performed using Bayesian and parsimony analyses of six plastid DNA regions and a broad sampling of genera from all tribes of the subfamily. In the inferred phylogenetic hypotheses, the tribal relationships were mostly well supported, with Ixoroideae consisting of the Coffeeae and the Vanguerieae alliances as sister groups and a grade comprising Condamineeae, Henriquezieae, Posoquerieae, Retiniphylleae, Sipaneeae and the genus Steenisia. A revised tribal classiﬁcation, including the description of ﬁve new tribes, Airospermeae, Augusteae, Scyphiphoreae, Steenisieae and Trailliaedoxeae, is provided. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406.
ADDITIONAL KEYWORDS: Airospermeae – Augusteae – molecular phylogenetics – Scyphiphoreae –
Steenisieae – systematics – Trailliaedoxeae.
With >13 000 species (Davis et al., 2009), Rubiaceae is one of the largest and most diverse families of angiosperms. Well-known representatives include Coffea L., Ixora L. and Gardenia J.Ellis, all part of Ixoroideae, a subfamily comprising about 4000 species of pantropical and subtropical distributions. Ixoroideae, as recognized by Bremekamp (1952, 1966), included taxa characterized by secondary pollen presentation (‘ixoroid pollination mechanism’), a feature that Bremekamp considered to be of high taxonomic value because of its requirement for a combination of characters for functionality. Included were tribes Acranthereae, Chiococceae, Coptosapelteae, Cremasporeae, Gardenieae, Ixoreae and Vanguerieae. Verdcourt (1958), however, considered pollen presentation to be of less importance, and preferred to
*Corresponding author. E-mail: firstname.lastname@example.org
include Ixoroideae in a wide Cinchonoideae (see also Robbrecht & Manen, 2006). In a comprehensive classiﬁcation of the family, Robbrecht (1988) restricted Ixoroideae to include genera with contorted corolla lobe aestivation and ﬂeshy fruits. In his system, Ixoroideae comprised tribes Cremasporeae, Gardenieae and Ixoreae sensu Bremekamp (the correct name of which would have been Coffeeae; Darwin, 1976), i.e. Aulacocalyceae, Coffeeae, Gardenieae, Octotropideae and Pavetteae. For an overview of the changes in the classiﬁcation of Ixoroideae, the reader is referred to Andreasen & Bremer (2000). Results of molecular phylogenetic studies have since then indicated many unknown relationships and also, consequently, possible improvements in the classiﬁcation of Rubiaceae. This includes the expansion of Ixoroideae, as many additional tribes or segregates of tribes and a number of taxa of uncertain taxonomic placement have been shown to be associated with the subfamily. Ixora, the type of the subfamily, was shown
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
K. KAINULAINEN ET AL. Kainulainen et al., 2009; Razaﬁmandimbison et al., 2011). Subsequent tribal recognition of the lineages represented by these genera has so far only been performed for Aleisanthia and Aleisanthiopsis and Greenea (Aleisanthieae and Greeneeae, respectively; Mouly et al., 2009a). In this study, we analyse data from six combined plastid DNA regions (matK, ndhF, rbcL, the rps16 intron, trnS-G and trnT-F) using Bayesian and parsimony methods of phylogenetic reconstruction to resolve the tribal relationships of the expanded Ixoroideae and, in particular, the relationships of the genera which, in previous studies, have not been associated with any previously described tribes. Following the inferred phylogenetic hypothesis, we also provide a revised tribal classiﬁcation of the subfamily.
to form a clade with Vanguerieae (Bremer et al., 1999), conﬁrming the position of Vanguerieae in Ixoroideae, as suggested by Bremekamp (1952, 1966), and supporting the exclusion of Ixora from Pavetteae. Andreasen & Bremer (2000) resurrected Ixoreae and provided new circumscription for several other tribes in the subfamily. Many additional taxa have been found to be associated with Ixoroideae sensu Robbrecht (1988), including Bertiera Aubl. (Bremer, Andreasen & Olsson, 1995), Mussaendeae and Sabiceeae, (Bremer & Thulin, 1998), Alberteae and Scyphiphora C.F.Gaertn. (Bremer et al., 1999), Condamineeae and many genera formerly placed in Cinchoneae or Rondeletieae (e.g. Bremer et al., 1999; Rova et al., 2002; Delprete & Cortés-B., 2004; Kainulainen et al., 2010). Crossopteryx Fenzl, part of Ixoroideae sensu Bremekamp (included in Coptosapelteae), but considered part of Cinchoneae by Robbrecht (1988), has also been found to be nested in Ixoroideae (Razaﬁmandimbison & Bremer, 2001), as have Mussendopsis (Razaﬁmandimbison & Bremer, 2001), Hekistocarpa Hook.f. (Dessein et al., 2001), Gleasonia Standl., Retiniphyllum Humb. & Bonpl. and Sipaneeae (Rova et al., 2002; Delprete & Cortés-B., 2004), Boholia Merr. and Steenisia Bakh.f. (Bremer & Eriksson, 2009), Airosperma K.Schum. & Lauterb. (Kainulainen et al., 2009), Greeniopsis Merr. (Alejandro et al., 2010), Glionnetia Tirveng., Jackiopsis Ridsdale and Trailliaedoxa W.W.Sm. & Forrest (Razaﬁmandimbison et al., 2011). Although the expanded Ixoroideae is well supported by molecular data, internal resolution and clade support, especially among the early divergent clades, have generally been low. Ixoroideae, as widely delimited according to recent molecular phylogenetic studies, includes all tribes of Robbrecht’s (1988) narrow circumscription of the subfamily, whereas tribes Acranthereae, Chiococceae and Coptosapelteae are not part of Ixoroideae as suggested by Bremekamp (1966). Chiococceae has been shown to be part of Cinchonoideae (Bremer et al., 1995), and Acranthera Arn. ex Meisn. and Coptosapelta Korth. appear to represent a separate, early divergent clade in the family (Rydin et al., 2009). The expanded Ixoroideae is morphologically diverse and can no longer be easily characterized morphologically. Molecular phylogenetic studies have also shown that some tribes of the subfamily are not monophyletic (i.e. Gardenieae including Aulacocalyceae, and Pavetteae; Andreasen & Bremer, 2000; Persson, 2000; Bremer & Eriksson, 2009) and that several genera found to be nested in Ixoroideae do not appear to be associated with any described tribe, i.e. Airosperma, Aleisanthia Ridl., Aleisanthiopsis Tange, Augusta Pohl, Boholia, Glionnetia, Greenea Wight & Arn., Scyphiphora, Steenisia, Trailliaedoxa and Wendlandia Bartl. ex DC. (Rova et al., 2002; Bremer & Eriksson, 2009;
MATERIAL AND METHODS TAXON SAMPLING
This study includes genera representing all tribes associated with Ixoroideae in previous molecular phylogenetic studies. The ingroup included 110 species from 87 genera. An effort was made to sample primarily material representing the types of genera. Gelsemium sempervirens (L.) J.St.-Hil. (Gelsemiaceae), Logania vaginalis (Labill.) F.Muell. (Loganiaceae), Luculia gratissima (Wall.) Sweet, Colletoecema dewevrei (De Wild.) E.M.A.Petit, Ophiorrhiza mungos L. and six species of Cinchonoideae were utilized as outgroup. Because the focus of the study is primarily concerned with the phylogeny of the early divergent lineages of the subfamily, sampling was limited in the large and problematic Gardenieae and associated tribes (Octotropideae and Pavetteae), the phylogeny of which will be investigated further in an upcoming study (A. Mouly et al., Université de Franche-Comté, Besançon, unpubl. data). Sampling was increased for Airosperma, Augusta and Wendlandia, all of which have widely disjunct distributions and in previous molecular phylogenetic studies have been resolved in Ixoroideae, but not in association with any previously recognized tribes (Rova et al., 2002; Kainulainen et al., 2009). We were able to obtain sequences of Airosperma taxa from New Guinea and Fiji, including A. trichotomum (Gillespie) A.C.Sm., originally described as Abramsia trichotoma Gillespie. The Augusta sample comprised specimens of the type A. longifolia (Spreng.) Rehder from Brazil, A. austrocaledonica (Brongn.) J.H.Kirkbr. from New Caledonia and A. rivalis (Benth.) J.H.Kirkbr. from Central America, the last two species of which were previously recognized as Lindenia Benth. The Wendlandia sample included W. arabica Deﬂers and W. ligustroides (Boiss. & Hohen.) Blakelock, the inclusion of
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
Botanical Journal of the Linnean Society.99. RESULTS The combined dataset contained 10 003 DNA characters. 1320F and 2280R (Rydin. 2002. 2002) and rpsR2 (Oxelman. 720F. with the exception of the position of Randia L. 2003)...5. 9082–9113. a script dependent on the program PHYML v3. An overview of the sampling and voucher specimens is given in the Appendix. Higgins & Gibson. Sequences were assembled using the Staden package v1.95. but was resolved as sister group to a clade comprising Rosenbergiodendron Fagerl.5 (Rambaut & Drummond. plastid genome (GenBank accession number. AMPLIFICATION AND SEQUENCING Three protein coding genes (matK. Analyses of the coding and noncoding datasets separately (data not shown) showed no incongruences with bootstrap support (BS) values Ն70% or PPs Ն 0. The initial 25% of the sampled trees were considered as burn-in and excluded from the consensus. Clade support was estimated using 1000 bootstrap replicates. (PP. eF. Yang & Rannala. pleurocarpa (Airy Shaw) Bakh. and cF. 9330–9335 and 9714–9723 (trnS-G) of the © 2013 The Linnean Society of London. Substitution models suggested as best ﬁt to the data under the corrected Akaike information criterion (AICc). Andersson & Antonelli.f. The inferred phylogenetic hypotheses of the MP and BI DATA ANALYSES The sequences were preliminarily aligned using Clustal W (default settings. ndhF and rbcL) and three noncoding regions [the rps16 intron. Inversions in the included sequences occurred in regions corresponding to positions 5417–5430 (rps16). 2002) and MrBayes v3.PHYLOGENY OF IXOROIDEAE which in Wendlandia was considered to be doubtful in the last comprehensive revision of the genus by Cowan (1932). 0. 1994). Additional sequences (361) were obtained from GenBank (for references. Kainulainen et al. 1991).0b10 (Swofford. EF044213. see Appendix). An AT-rich region in the trnS-G spacer. 2007). Bremer et al. The analysis comprised two runs of four chains each and was monitored for 107 generations. For the BI analyses. The combined dataset consisted of 10 165 characters. 820R. was excluded from the analyses because of difficulties in ﬁnding an unambiguous alignment. 387–406 .4. with three random addition replicates per replicate. 2005) for matK. 1999). 2410 of which were potentially phylogenetically informative in the MP analysis.. Methods of phylogenetic reconstruction included maximum parsimony (MP) and Bayesian inference (BI. The chain heating parameter was 0. PCR ampliﬁcations were performed using standard PCR settings and the following primers: matK1198F and matK2053R (Andersson & Antonelli. 0. Razaﬁmandimbison & Bremer. and then adjusted manually. 389 DNA EXTRACTION. with every 1000th generation being sampled. Samson et al. 2001. Lidén & Berglund. Coffea arabica L. as recommended by Drummond et al. 1997). rbcL_Z895F.. as implemented in BioEdit (Hall. 2005. (2007) for the adequate representation of the posterior probability (PP). 2002).4 (Nylander. 1997) for the rps16 intron.. the trnS-G spacer including the trnG intron (trnSGCUtrnGUUC-trnGUUC) and the trnT-F region (trnTUGUtrnLUAA-trnLUAA-trnFGAA)] of the plastid DNA. and Tocoyena Aubl. 2004. 9164– 9169. in order to ensure an ESS > 200. MP analyses were performed using heuristic searches with the tree bisection–reconnection (TBR) branch swapping algorithm. Multrees on.. 2002) for rbcL. other than S. 1999.95. DNA was extracted from leaf material using a MiniBeadbeater 3110BX (BioSpec). in the noncoding dataset (PP.. which formed a sister group to Euclinia Salisb. 2002. Sequence inversions were dealt with by separating the alternative sequence versions in the alignment. We were unsuccessful in obtaining DNA sequences from any Steenisia spp. Guindon & Gascuel. and was subsequently puriﬁed using the QIAquick® PCR puriﬁcation kit according to the manufacturer’s instructions (Qiagen). 2009).. were used in this study. 2007). and a few species representing the different tribes of Ixoroideae are shown in Figure 1.2 (Huelsenbeck & Ronquist. The trnS-G region was ampliﬁed using the primers and protocols of Shaw et al. A1F. 1996). as implemented in MrAIC v1. BS. Sequences new to this study (324) were deposited in GenBank (Appendix). 2013. 2003). Ronquist & Huelsenbeck. previously shown to be phylogenetically informative in Rubiaceae (Andersson & Rova.10. 940F.0. corresponding to positions 9184–9203 of the C.3 (Staden. fR (Taberlet et al. the protein coding and noncoding data were analysed as separate partitions with unlinked model parameter estimates (except topology). 73%) in the coding dataset. respectively. 173.. following the protocol of Doyle & Dickson (1987). rsp16_2F (Bremer et al. Thompson.1. 1000R. 2F. Gaps were treated as missing data. 10 003 of which were included in the analyses. 1250F. (2005). The effective sample sizes (ESSs) of the model parameters were checked using the program Tracer v1. BS. rbcL_Z895R and rbcL3’R (Bremer et al. IR (Bremer et al. using the programs PAUP* v4. 2008) for ndhF. were used for each partition (the GTR + G + I model for both datasets). 1000 random sequence addition replicates and a maximum of 10 trees saved per replicate. Rova et al. 84%). dR. rbcL5’F. 1880F and 2670R (Rydin et al. arabica plastid genome.. 1700R. 2008) for trnT-F. Razaﬁmandimbison & Bremer. 1999.
Augusta rivalis. Scyphiphora hydrophylacea. Bertiera rufa. Tropicos. by Indiana Coronado. 387–406 . N. © MBG. C.390 K. H. L. botanical information system at the Missouri Botanical Garden – http://www. University of Vienna.0 licence). H. E. 2013. 173. Steenisia pleurocarpa.tropicos. G. Botanical Journal of the Linnean Society. Sabicea diversifolia. I. M. © 2013 The Linnean Society of London. K. D. E. Pavetta sp. Selected taxa of Ixoroideae: A. A B C D E F G H G I J K J L M N Figure 1..org. K–N. F. Faculty Centre of Biodiversity. G. Glionnetia sericea. F. KAINULAINEN ET AL. Rosenbergiodendron densiﬂorum (image credits: A–D. Schizomussaenda henryi. used with permission. J. Mitriostigma axillare. B. Bremeria pervillei. licensed under a Creative Commons by-nc-nd 3. Posoqueria longiﬂora. Ixora borboniae. Wendlandia tinctoria. J. © Christian Puff. by Kent Kainulainen. I.
(2008). 1.Li (Fig. 85%). 391 DISCUSSION In this study.00. and Oxyanthus DC.00. 97%) and Crossopteryx (PP. 100%) and an Airosperma–Boholia clade (PP. 173. respectively (cf. 72%).. BS. including the PPs of the clades and the clade BS values of the MP analysis. Relationships between the Aleisanthieae– Greeneeae–Ixoreae clade.79. the support for this clade was low (PP. As in previous studies (Rova et al. in turn.00. and Mussaenda L. Phylogenetic relationships in this tribe should be investigated further. 2013. Gardenieae did not appear to be monophyletic. 0. (2001). 0. Cortés-B. 100%) and a clade comprising the sister tribes Mussaendeae and Sabiceeae (PP. 2009. 1. in turn. BS. although with weak support (PP. (subfamily Rubioideae) by Bakhuizen van den Brink (1952). as in previous studies by Bremer & Thulin (1998) and Khan et al. the support for this trichotomy was low in the MP analysis (< 50%). and a clade comprising Bertiereae and Coffeeae (PP. Octotropideae and Pavetteae and the genera Airosperma. The Gardenieae–Pavetteae clade was resolved as sister group to the Burchellia– Octotropideae clade (PP. sister group to the remainder of the subfamily. BS.00. Delprete & Motley (2009) have subsequently demonstrated the monophyly of the monogeneric Retiniphylleae. based on molecular data) by Dessein et al.PHYLOGENY OF IXOROIDEAE analyses were overall mostly congruent. Heinsia DC. Trailliaedoxa was resolved as sister to the clade formed by this trichotomy. & Alejandro (Fig. sister to Greeneeae (PP. 1.00. 54%). However. in which Hekistocarpa instead forms a poorly supported sister group to Sabicea Aubl. Mussaendeae is resolved as sister group to Sabiceeae with strong support. 54%). Razaﬁmandimbison et al. were resolved as sister groups (‘the core Ixoroideae’. 2011). 1. 1. 1C) and Landiopsis Capuron ex Bosser.00. Coffeeae. 87%). 100%). 100%). this clade also had low support (PP. 1. In the phylogenetic tree presented. in their study. The position of Retiniphyllum indicated in this study conforms with that ﬁrst found in the study by Rova et al. 1. Although strongly supported by the BI analyses (PP. well resolved and strongly supported. BS.Br. Botanical Journal of the Linnean Society. BS. 1. 91%). Boholia and Wendlandia. 2010). as in the study by Rova et al. These relationships are not supported in our study. 100%) and this clade was. 1. BS. In a © 2013 The Linnean Society of London.00. 96%). The clades corresponding to the Coffeeae and Vanguerieae alliances. Vanguerieae and Glionnetia were unresolved.98. A Condamineeae–Henriquezieae–Posoquerieae– Sipaneeae clade was resolved as the earliest diverging clade in relation to the rest of the subfamily. As. (2002). BS. the Vanguerieae alliance and a grade consisting of Retiniphylleae... Subfamily Ixoroideae received strong support (PP.. The phylogenetic hypotheses indicate that Ixoroideae can be considered as comprising the Coffeeae alliance. was resolved as sister group to Octotropideae (PP. Schizomussaenda H. 1. Augusta.00. (2002). Kainulainen et al. Steenisia. A grade of successive sister clades to core Ixoroideae comprised. Mussaendeae with Sabiceeae and a Condamineeae–Henriquezieae–Posoquerieae– Sipaneeae clade (Fig. The Coffeeae alliance comprised the tribes Alberteae. 0. 2). BS. BS. 1. Razaﬁmandimbison & Liede-Schumann (2005). 1B) from South-East Asia is here further resolved as sister group to a clade comprising the Malagasy–Mascarene genera Bremeria Razaﬁm. BS 100%). Jackiopsis (PP.. forms a sister group to the remaining genera of the tribe.00. in the phylogenetic hypotheses of Kainulainen et al. The Mussaendeae– Sabiceeae clade was well supported (PP. Bremer & Eriksson. previously. 100%). 54%).00. formed a sister group to Pavetteae. Retiniphylleae (PP. BS. 64%). Posoquerieae and Sipaneeae form a clade. 387–406 . 1. 1. an Augusta–Wendlandia clade (PP. Strongly supported successive sister groups were Alberteae (PP.l. forms a clade with Pseudomussaenda Wernham. Figure 2 shows the majority rule consensus tree from the BI analyses of the combined data. we infer the tribal relationships in Ixoroideae by the phylogenetic reconstruction of six combined plastid regions.83.. Henriquezieae. BS. is resolved as sister group to Tamridaea Thulin & B. These genera. 100%). 0. (2009). 2002. 1. BS. and Mitriostigma Hochst. BS.L. BS. BS. 98%). have been suggested as constituting a clade recognized at tribal level (Virectarieae s. In Sabiceeae.Bremer.00. BS.00. Steenisia (PP. formed a sister group to this clade (PP.00. and the three genera also formed a well-supported clade in the study by Bremer & Eriksson (2009). Hekistocarpa has also been resolved as sister group to the remaining Sabiceeae (Khan et al. Further research is needed in order to better understand the relationships of these early divergent lineages. However. 1. BS. in turn. Bertiereae.00. BS. because Burchellia R.00).00. The South-East Asian genus Steenisia (Fig. Aleisanthieae formed a sister group to Ixoreae (PP. However.. In the Vanguerieae alliance. 1E) was segregated from Neurocalyx Hook. the resolution in Condamineeae was low. 2008. in turn.00. BS. Condamineeae appeared closer to core Ixoroideae. BS. together with Hekistocarpa. (2009). 1. PP. 65%). 100%). based on nrDNA data). Virectaria Bremek. However.80. This clade forms a weakly supported sister group to Condamineeae. Gardenieae. and the Condamineeae–Henriquezieae–Posoquerieae–Sipaneeae clade is. in agreement with the results of Alejandro.00. This is congruent with the results of Rydin et al. 1. 1. Successive sister groups were Scyphiphora (PP.
GAR Coddia rudis .00/66 0. Posterior probabilities and bootstrap support values from the parsimony analysis are indicated below the clades (a dash indicates bootstrap support of <50%). VAN. Bertiereae.MUS Schizomussaenda henryi .OCT Hypobathrum racemosum .CRO Jackiopsis ornata .GAR Mitriostigma axillaris . Henriquezieae.SIP Sipanea aff.00/98 1.00/ 1. CRO.00/100 1.00/100 1.00/100 Ixoroideae 1.SAB Sabicea aspera .00/100 1. RET.GAR Rosenbergiodendron densiflorum . Sipaneeae. 387–406 . 2013.80/72 1.PAV Pavetta indica .COF Coffea arabica .00/99 1.00/99 1.PAV Tennantia sennii .00/100 1.80/54 1.00/ 100 1.90/51 1.POS Posoqueria longiflora .OCT Paragenipa lancifolia .COF Coffea ebracteolata . GAR.SIP Pinckneya bracteata . © 2013 The Linnean Society of London.OCT Oxyanthus speciosus .VAN Multidentia concrescens .ALE Aleisanthiopsis distantiflora .00/100 1.SAB Tamridaea capsulifera .CON Simira cordifolia .VAN Rytigynia senegalensis .98/74 1. trnS-G and trnT-F).00/- 1.SIP Neobertiera gracilis .BER Bertiera aethiopica .SIP Dendrosipanea spigelioides .99/84 0.00/94 Vanguerieae Airospermeae Augusteae Bertiereae Coffeeae Octotropideae Pavetteae Gardenieae 1.VAN Keetia gueinzii .54/1.COF Coffea sessiliflora .GAR Atractocarpus balansaeanus .ALE Ixora novoguineensis .00/97 1. PAV.OCT Feretia apodanthera .GAR Catunaregam spinosa . rbcL. Octotropideae. BER.00/64 1. Phylogram of the tree with the highest marginal likelihood in inset.00/100 1.00/100 0. KAINULAINEN ET AL. MUS. Retiniphylleae.392 K. Alberteae.GAR Pavetta abyssinica .00/100 0.CON Calycophyllum candidissimum .CON Condaminea corymbosa .VAN Vangueria madagascariensis .MUS Mussaenda arcuata .SAB Hekistocarpa minutiflora .00/99 1. Coffeeae.CON Emmenopterys henryi . Vanguerieae.00/100 1.79/72 1. 173.00/97 1.IXO Ixora margaretae .RET Crossopteryx febrifuga .GAR Hyperacanthus grevei .00/100 1.00/ 100 1.IXO Ixora ferrea . GRE. Posoquerieae.CON Hippotis triflora . Greeneeae.00/100 1.SIP Sipanea hispida .IXO Ixora borboniae . Aleisanthieae.CON Chimarrhis hookeri .00/100 1.02 Figure 2.MUS Landiopsis capuronii .SAB Sabicea diversifolia .92/68 0.SAB Heinsia crinita .00/96 1. COF.87/1.00/100 1. Gardenieae.00/100 Sabiceeae Mussaendeae Retiniphylleae Aleisanthieae Ixoreae Trailliaedoxeae 0. Sabiceeae. SIP.GAR Aoranthe penduliflora .97/56 1.82/- 0.00/100 1.00/83 Coffeeae-alliance 1.VAN Psydrax obovata . Condamineeae.00/100 1.POS Chalepophyllum guyanense .GAR Randia aculeata . Gelsemium sempervirens Logania vaginalis Luculia gratissima Colletoecema dewevrei Ophiorrhiza mungos Cinchona pubescens Rondeletia odorata Guettarda speciosa Cubanola domingensis Cephalanthus occidentalis Nauclea orientalis Henriquezia nitida .65/0.00/98 0.VAN Fadogia tetraquerta . HEN.00/87 1.00/98 100 1.CON Dioicodendron dioicum . Mussaendeae.00/100 1.00/83 1.00/100 1. SAB.MUS Mussaenda erythrophylla .GAR TRAILLIAEDOXEAE SCYPHIPHOREAE STEENISIEAE AUGUSTEAE AIROSPERMEAE 0.00/92 Vanguerieae-alliance 1. biflora . ALE.GAR Aulacocalyx jasminiflora . Airosperma psychotrioides Airosperma trichotomum Airosperma vanuense Augusta austrocaledonica Augusta longifolia Augusta rivalis Wendlandia ligustroides Wendlandia formosana Wendlandia tinctoria Wendlandia arabica Wendlandia paniculata Alberta magna . ALB.GAR Tocoyena pittieri . Botanical Journal of the Linnean Society. New tribal names presented in this article are highlighted.00/100 1.GRE Aleisanthia rupestris .CON Bathysa stipulata .00/100 1.GAR Duperrea pavettifolia .00/91 0.GAR Euclinia longiflora .MUS Bremeria landia .00/88 0.OCT Fernelia buxifolia .BER Empogona coriacea .00/100 1.98/54 1. IXO.CON Pogonopus speciousus .00/100 core Ixoroideae 1. rps16 intron.00/100 0.97/85 1.90/1. Pavetteae.PAV Coptosperma supra-axillare .00/87 0.00/ 100 1.MUS Steenisia pleurocarpa Retiniphyllum pilosum .00/97 1.GAR Gardenia hansemanni .PAV Genipa americana .POS Posoqueria latifolia .00/98 1.93/59 1.00/100 1.00/100 1. Jackieae.VAN Peponidium horridum . CON.CON Mastixiodendron flavidum .SAB Sabicea africana .VAN Cyclophyllum deplanchei .00/100 1.00/100 0.00/100 0.VAN Boholia nematostylis Airosperma sp.00/ 100 1.00/100 0.COF Burchellia bubalina .00/100 1.00/ 100 1.00/ 100 0.00/100 0.00/100 0.00/ 100 1.VAN Pyrostria hystrix .61/- 1.00/100 1.00/100 1.00/83 1. OCT.IXO Canthium coromandelicum .CON Virectaria multiflora . Crossopterygeae.GAR Rothmannia capensis .00/88 0.ALB Bertiera guianensis .86/- 1.BER Bertiera longithyrsa .00/100 1.00/100 Henriquezieae Posoquerieae Sipaneeae Condamineeae 1. The majority-rule consensus tree from the Bayesian inference analysis of the combined plastid data (ndhF.94/73 1.00/100 1.00/100 1.HEN Molopanthera paniculata .JAC Scyphiphora hydrophylacea Trailliaedoxa gracilis Glionnetia sericea Greenea oblonga .00/100 1.00/100 1.CON Rustia thibaudioides .CON Ferdinandusa speciosa .00/100 1.00/65 0.MUS Pseudomussaenda flava .00/96 1.54/72 1.00/100 1.IXO Ixora trilocularis .VAN Afrocanthium lactescens .00/100 0.00/100 1.GAR Cremaspora triflora .IXO Ixora coccinea . matK.00/91 1.00/76 1.GAR Kailarsenia tentaculata .00/85 1.00/95 1. JAC.00/76 1.00/100 1.00/100 1. Ixoreae.83/54 1.65/50 1. POS.
the ﬂowers have secondary pollen presentation and leftcontort corolla aestivation.Phillips and a clade comprising Cyclophyllum Hook. pollen is not presented in a secondary manner. However. although with an unresolved position relative to Vanguerieae and the Aleisanthieae–Greeneeae–Ixoreae clade (Rondeletieae s. Crossopterygeae. Manns & Bremer. Steenisia was found nested in Ixoroideae. Consequently. 1984). Scyphiphora. 387–406 . representing the ‘dioecious group’ of Razaﬁmandimbison et al. is here further resolved in a clade consisting of Afrocanthium (Bridson) Lantz & B. (1999). characters which are all unusual (the latter unique) in Ixoroideae. the position of Psydrax Gaertn. 1984. Glionnetia (Fig. Trailliaedoxa and Vanguerieae. Whether or not secondary pollen presentation occurs is not known. Jackieae and Crossopterygeae. Steenisia is not associated with any previously described tribe in our analyses and.Bremer. However. The fruits are indehiscent and corky. in particular. an endemic of the Seychelles. 2010). Scyphiphora was resolved as sister to the Ixoreae– Vanguerieae clade. Further research is needed to better understand the phylogenetic relationships in the Gardenieae– Octotropideae–Pavetteae complex. cf.. Jackieae. in turn. 2013. It occurs in the highlands of southern China. sister to Greeneeae.f. However. Andreasen & Bremer (2000) tentatively included the genus in Ixoreae.) Arènes and Pyrostria Comm. Scyphiphora has a complex taxonomic history (see Puff & Rohrhofer. Ixoreae. 2009). has also been suggested as part of Rondeletieae by its author (Tirvengadum. Instead. Successive sister groups to this complex are the Bertiereae–Coffeeae © 2013 The Linnean Society of London. (2009). However. we propose the recognition of tribe Scyphiphoreae (see Taxonomic synopsis section).. (2009). characteristics shared by most of the core Ixoroideae. Coffeeae. Mitriostigma (Fig. A region of the style covered with hairs that probably catch released pollen is usually found level with the pollen sacs (Bremer. in the molecular phylogenetic study of Bremer & Eriksson (2009). and these are. Boholia. Glionnetia was found nested in the Vanguerieae alliance. ex Juss. (2002) and Mouly et al. the recognition of the Steenisia clade at the tribal level is proposed in the Taxonomic synopsis section. Our results support the recognition of a monogeneric tribe. with one ascending and one descending ovule per locule (Puff & Rohrhofer. 173. Mouly et al.. 2009). Trailliaedoxa is an erect shrublet with minute schizocarpic fruits with solitary pendulous ovules. Rova.. 1873).). Steenisia can be readily characterized by a suffrutescent unicaulous habit. Despite the inclusion of more sequence data in this study. although it has rarely been collected. Trailliaedoxeae (see Taxonomic synopsis section). Bremer (1984) proposed that it should be transferred from Argostemmateae to Rondeletieae (subfamily Cinchonoideae). the mode of pollination is most likely by buzz pollination (Puff et al. in which Scyphiphora is resolved as sister to the Aleisanthieae–Glionnetia–Greeneeae–Ixoreae– Trailliaedoxa–Vanguerieae clade. 1996. which are adapted for sea dispersal. The corolla aestivation is leftcontort. 2009a). Gardenieae. 1995). Botanical Journal of the Linnean Society. consequently. Greeneeae. The clades resolved in Vanguerieae in this study are congruent with the results of Lantz & Bremer (2004).. Octotropideae and Pavetteae. Puff et al.s. As in the study by Razaﬁmandimbison et al. THE COFFEEAE ALLIANCE The Coffeeae alliance comprises Airosperma. as this region does not appear to extend above the surrounding staminal tube. 1993). successive sister groups to the Aleisanthieae– Glionnetia–Greeneeae–Ixoreae clade are Trailliaedoxa.. The little-studied Trailliaedoxa has hitherto remained without taxonomic placement in Rubiaceae. 1993). 2010. Delprete & Bremer. 1G). (2011). Bremer & Eriksson (2009) and Cortés-B. have caused difficulties in assessing its systematic placement. The mangrove plant Scyphiphora (Fig. in a recent study by Razaﬁmandimbison et al. as the highly modiﬁed fruits. 1993. can consequently be consid- ered as restricted to the New World.PHYLOGENY OF IXOROIDEAE revision of the genus. rotate corolla and anthers with apical appendages fused to form a hollow cone around the style (in a manner reminiscent of the ﬂowers of Solanum L. and Burchellia forms a sister group to Octotropideae. As in previous molecular studies (Andreasen & Bremer. Glionnetia. Scyphiphora. (2009a). the phylogenetic position of Glionnetia is still unresolved. Bremer & Eriksson. Keetia E. 1F) occurs in coastal areas of tropical Asia and the western Paciﬁc (Puff & Rohrhofer. a position congruent with this study. 1M) and Oxyanthus form a poorly supported sister group to Pavetteae. 2002. However. In agreement with the results of Rova et al. Peponidium (Baill. (2011). Augusta. 1995). a tribe characterized by contorted or imbricate corolla aestivation and capsular fruits. Ixoreae forms a sister group to Aleisanthieae. and Rondeletieae has since been much reduced (see Rova et al. et al. Molecular phylogenetic studies have indicated that this is an unnatural group. in the studies by Bremer et al. 393 THE VANGUERIEAE ALLIANCE The Vanguerieae alliance comprises Aleisanthieae. However. Gardenieae is not monophyletic. Wendlandia and tribes Alberteae. Manns & Bremer. Aleisanthia and Greenea both have traditionally been considered part of Rondeletieae (Hooker.
which will be discussed further by A. The status of this character in Augusta is not known. unpubl. a relationship also inferred in other studies (e. they were resolved as a clade in Ixoroideae. Both genera have left-contorted corolla aestivation. Both genera have widely disjunct distributions. data). Guangdong. 1979) and at least some of the New Guinean species of the genus appear to be functionally dioecious (Darwin. (2002). W. 1949) and Henriquezia Spruce ex Benth. at times. pers. in Dialypetalanthaceae (Rizzini & Occhioni. included species from the respective areas form sister groups). Dialypetalanthus Kuhlm. in which W. because A.P. The included representatives of Bertiera form a monophyletic group sister to Coffeeae. image seen). Somalia and Yemen (see Puff.394 K. with one species.). W. monocaulous treelets. white or yellow. in Henriqueziaceae (Bremekamp. Stipules entire. 173. austrocaledonica are paraphyletic with respect to A. we propose that it should be recognized at tribal level (see Taxonomic synopsis section).. The fruits are ﬂeshy and contain pyrenes. animal dispersal also seems a possibility considering the vivid colour of the fruits (blue–purple.g. 2000.H. which some authors have treated as one..) J. vitiensis (Seem. occurring in New Guinea and the Fiji islands (in the phylogenetic hypothesis. the TAXONOMIC SYNOPSIS Following the results of the molecular phylogenetic analyses. A. ligustroides. 1900. 2013. we propose that this clade should be recognized at the tribal level (see Taxonomic synopsis section). & Bonpl. Kainulainen. observ. Davis et al. This synonymization is supported by the molecular data. 1995. Although the molecular support for Ixoroideae is strong. ﬁve of which are newly and formally described below. some of which. the corolla aestivation is left-contorted in both genera (K.e. 1873) been considered as part of Rondeletieae. Merrill. (Université de Franche-Comté. However. 2000. Darwin. the Augusta–Wendlandia clade and the Airosperma–Boholia clade. Secondary pollen presentation is not present in Airosperma (Darwin. Gardenieae. Octotropideae (including Cremasporeae) and Pavetteae. in southeastern Turkey–northern Iraq and one species. arabica. consequently. In this study. However. 2). P. subshrubs or rarely herbs. and were interpreted by Robbrecht (1988) as adapted for dispersal by sea currents. 1957)]. morphologically the members are diverse and not easily characterized. ligustroides forms a sister group to the remaining included species. Persson. Guangzhou. Condamineeae and Henriquezieae contain morphologically aberrant genera (Rogers. because A. Boholia occurs in the Philippines. Robbrecht & Manen.g. Smith (1945: 108) considered the generic concepts as ‘essentially identical’ and subsumed Abramsia. Raphides absent. Augusta and Wendlandia have traditionally (Hooker. 1926) based on the presence of solitary pendulous ovules and contorted corolla aestivation. Alberteae. Mouly et al. Botanical Journal of the Linnean Society. KAINULAINEN ET AL. and their inclusion in Wendlandia as doubtful. This clade is not associated with any previously described tribe. In particular. Airosperma has a disjunct distribution.. vanuense S. SUBFAMILY IXOROIDEAE RAF. no potential morphological synapomorphies for the subfamily are known at this point. The last three species have previously been recognized as Lindenia. in the molecular phylogenetic study of Rova et al. shrubs. consequently. we present here a revised tribal classiﬁcation of Ixoroideae. comm. However. see the latter for a discussion on the delimitation and morphological differentiation of these tribes. A. Including these three tribes. Although having been described as right-contorted or imbricate. arabica is nested in the East Asian clade. as in that of Kainulainen et al. 1J) has a wide distribution in East Asia and Australasia (centre of diversity in China). This is supported by our results. and Platycarpum Humb. 2). in Ethiopia. i. 2006). who provided the last comprehensive revision of the genus. have been classiﬁed outside Rubiaceae [e. 1980). South China Botanical Garden. rivalis (Fig.Darwin (Fig. 1990). 1980).Kirkbr. Zhang. trichotomum. Andreasen & Bremer. trichotomum is nested in Airosperma. was originally described by Gillespie (1932) as Abramsia trichotoma. A. they form a clade separate from Alberteae. Wendlandia appears to be monophyletic in our phylogenetic analyses. Bremer et al.). but has also been collected on the island of Flores in Indonesia (Schmutz 2691. a name that was reduced to synonymy by Kirkbride (1997). 1984.e. Kainulainen et al. 387–406 . Ixoroideae comprises 24 tribes. In the Coffeeae alliance. although we do not address the tribal delimitation in the problematic Gardenieae complex. A. whereas W. pers. rivalis and A. Airosperma and Boholia were placed in Alberteae by their respective authors (Schumann & Lauterbach. In Augusta. 1I) in Central America. One of the Fijian species. 2010). (2009). Trees. considered the last two species as exceptional. forming a sister group to A. clade. Cowan (1932). China. 2007. in Fiji. Secondary pollen presentation appears to be absent in Wendlandia (D. biﬁd © 2013 The Linnean Society of London. 1997). longifolia (Fig. Besançon. The status of this character in Boholia is not known. Wendlandia (Fig. the Augusta–Wendlandia clade is distinguished by capsular fruits. longifolia occurs in northeastern and central Brazil (Delprete. i. austrocaledonica in New Caledonia and A.
Tribe Augusteae Kainul. dry and indehiscent or capsular. Type: Airosperma K. with left-contorted aestivation. Style exserted. rarely to right. complanata. Type: Augusta Pohl. with septicidal (Augusta) or loculicidal (Wendlandia) dehiscence. Calyx persistent. shrubs or small trees. Südsee: 565 (1900) Suffrutices. Discospermum © 2013 The Linnean Society of London. trib.Bremer. Corolla tubulari-infundibuliformis. Shrubs to small trees. (2010). with one pendulous ovule in each locule. ovulis numerosis horizontaliter insertis. and Wendlandia (c. & B. lobis in aestivatione sinistrorsum contortis. Tribe Coffeeae DC. in maturitate azureopurpurei. testa reticulata.f. (2009): Nematostylis Hook. Madagascar. & Lauterb. For a description. Fruits capsular. Bertiereae as currently deﬁned is monogeneric. few or solitary ovules per locule. rarely zygomorphic. Flowers usually actinomorphic. 2: 1 (1828) Frutices vel arbusculae. Calyx persistens. (2009). 80 spp. Included genera (here investigated): Alberta. heterostylous. Distribution: Tropical Africa. (2007). with left-contorted aestivation. compressed. 173. Included genera (here investigated): Coffea and Empogona. and the monotypic Boholia from the Philippines and the island of Flores. Distribution: South-east Africa and Madagascar. 2013. Inclusion based on Davis et al. Corolla tubular-funnel-shaped. South-East Asia and northern Australia. inclusion of Psilanthus Hook. Ovary bilocular. ovulo uno pendulo in quoque loculo. Ovarium biloculare.f. Flores 5-meri. Stylus exsertus.. albidi vel lutescentes. Fructus carnosi. Included genera (here investigated): Aleisanthia and Aleisanthiopsis..) and Davis et al. Flowers 5-merous. Corolla short. Included genera: Airosperma with six species in Fiji and New Guinea. (2010): Greeniopsis. Pl. Distribution: Tropical South America to southern Mexico. Ovarium biloculare. Corolla brevi.. resurrection of Empogona Hook. Tribe Alberteae Hook. (2009. nov. Corolla aestivation contorted to left. Robbrecht (1988) and Kainulainen et al. with reticulate testa. Comores. Recent taxonomic changes have been made by Tosh et al. interpetiolar or rarely intrapetiolar. Belonophora Hook. Seychelles and tropical Asia to Australia. whitish or yellowish in maturity. nov. the Fiji islands and New Caledonia. 387–406 . becoming blue– purple. often with secondary pollen presentation. Included based on Kainulainen et al. Indonesia. tropical Africa. Stylus inclusus vel (longi-) exsertus. Diplospora DC. Bras. Tribe Aleisanthieae Mouly. Included genera: Augusta. Inﬂorescences terminal compound cymes or rarely corymbs.Bremer For descriptions. Madagascar and Mascarenes. in Coffea). with numerous ovules horizontally inserted. in several taxa with one or several lobes expanded and showy. Fruits ﬂeshy. Calyx persistens. Flores 5-meri in paniculis terminalibus. see Bridson & Verdcourt (2003). lobis in aestivatione sinistrorsum contortis. Flowers 5-merous in terminal panicles. with four species occurring in Mexico.Bremer. Tribe Airospermeae Kainul. see Mouly et al. Semina minuta. (1984). (2011. Descr. frutices vel arbusculae unicaules. Included genus: Bertiera. Distribution: South-East Asia. occurring in north-eastern Africa. Fl. Seeds minute.f. Calyx persistent.PHYLOGENY OF IXOROIDEAE or rarely ﬁmbricate.Schum. Fructus capsulares. trib. west Asia. monoecious or protogynous. pyrenis duabus. Schutzgeb.vel longi-tubularis.Florence & B. 395 Inclusion based on Alejandro et al. Inﬂorescentiae cymae terminales compositae aut raro corymbi. For descriptions..f. Fruits ﬂeshy and indehiscent. protandrous. with two pyrenes. Mascarenes. Icon.). dehiscentia septicida (Augusta) aut loculicida (Wendlandia). & B. see Davis et al.Bremer. Style included to (long-)exserted. (2007): Argocoffeopsis Lebrun. Tribe Bertiereae Bridson For a description. Botanical Journal of the Linnean Society. imbricate. valvate or rarely open.f and Razaﬁmandimbisonia Kainul.to long-tubular. with numerous. occurring in South-East Asia. & B. see Puff et al. Calyces mostly persistent. north-eastern and central Brazil. Calycosiphonia Pierre ex Robbr. (2009a) and Alejandro et al. Unicaulous subshrubs. J. Ovary bilocular. dioecious.
see Mouly et al.).f. Chimarrhis Jacq. b)... Distribution: Neotropics.. (2010).. Tribe Ixoreae A.. Ferdinandusa Pohl. Ixoreae as currently deﬁned is monogeneric.Presl. For a description. Capirona Spruce. (2005).f. Tribe Henriquezieae Hook. Included genera (here investigated): Bathysa C.). Included genera: Molopanthera Turcz. Inclusion based on Rogers (1984) and Delprete & Cortés-B.Bremer For a description.Rich. Distribution: Neotropics. Inclusion based on Tange (1994): Neomussaenda Tange. (2009a): Spathichlamys R.Gray. Parachimarrhis Ducke. & K.Andersson. Pentagonia Benth. Sommera Schltdl.. Dioicodendron Steyerm. Condaminea DC.. and Posoqueria Aubl. see Robbrecht (1988).396 K. Tribe Condamineeae Hook. 173. Seychelles. Included genera (here investigated): Henriquezia.) and the Malesia-Paciﬁc region (Dolicholobium A.Durand.. 2013. Included genus: Retiniphyllum. South-East Asia (Emmenopterys Oliv. Tribe Sabiceeae Bremek. Crossopterygeae as currently deﬁned is monogeneric.Florence & B. tropical Africa. see Khan et al. Hippotis Ruiz & Pav. and Mussaendopsis Baill. (2009a. south-eastern USA (Pinckneya Michx. Tribe Crossopterygeae F. Included genus: Crossopteryx. see Kainulainen et al. Bothriospora Hook. Calycophyllum DC.. carenes. see Alejandro et al.. ex DC.Schum. For descriptions.Gray. Included genus: Ixora. South-East Asia to the Paciﬁc. and Sri Lanka. Included genus: Jackiopsis.f. see Rogers (1984). Distribution: Tropical Africa. Madagascar. (2009a).f. Distribution: South-East Asia. (2008). Mussaendopsis. Distribution: Tropical South America. Mas- Dalzell. For a description. Madagascar.White ex Bridson For a description.Karst.. Botanical Journal of the Linnean Society. Warszewiczia Klotzsch and Wittmackanthus Kuntze.Parker.. Heinsia. Distribution: Neotropics. Included genera (here investigated): Bremeria. © 2013 The Linnean Society of London. KAINULAINEN ET AL. tropical Asia to the Paciﬁc. J.. Included genera (here investigated): Greenea. Distribution: Neotropics. Mastixiodendron. Landiopsis.f. Dolicholobium. Distribution: South-East Asia. see Mouly et al. Nostolachma T.Browne. Socotra. Dolichodelphys K. Inclusion based on Mouly et al. Holtonia Standl. 387–406 . (2011). Pseudomussaenda and Schizomussaenda. Comores. Retiniphylleae as currently deﬁned is monogeneric. and Platycarpum. Tribe Mussaendeae Hook. Inclusion based on Kainulainen et al. For a description. For a description. São Tomé. Mastixiodendron Melch. Sericanthe Robbr. and Xantonnea Pierre ex Pit. Tribe Greeneeae Mouly. Rustia Klotzsch and Simira Aubl.. see Bridson & Verdcourt (2003). Tribe Jackieae Korthals For descriptions. Tribe Posoquerieae Delprete For a description. see Delprete (2009).Krause. Tribe Retiniphylleae Hook. Distribution: Tropical South America. Mascarenes. Dialypetalanthus. Picardaea Urb. For descriptions. Tropical Africa. Tricalysia A. Semaphyllanthe L. Mussaenda. Pogonopus Klotzsch. (2004): Gleasonia Standl. see Ridsdale (1979) and Razaﬁmandimbison et al. Schizocalyx Wedd.. Emmenopterys. Tammsia H. Macbrideina Standl. Madagascar. Jackieae as currently deﬁned is monogeneric. Macrocnemum P. Pinckneya. (2010): Alseis Schott. Distribution: Tropical Africa. Elaeagia Wedd.
2013. Sipaneopsis Steyerm. Type: Trailliaedoxa W. with left-contorted aestivation. sometimes with one lobe expanding after anthesis. Corolla tubularis.. Flowers minute. Included genus: The monotypic Trailliaedoxa. Notes Roy. Anthers with extended apical appendages. & B. trib.Bremer. Pygmaeothamnus Robyns.f. Pteridocalyx Wernham. Style curved. Rytigynia Blume and Vangueria Juss. nov. Plectroniella Robyns. 387–406 .Sm. Fadogiella Robyns. with one ascending and one descending ovule in each locule.. with numerous ovules horizontally inserted.. Calyx persistens. Distribution: Southern Africa. with indistinct lobes. (2004). Dendrosipanea Ducke. Cyclophyllum. Ovarium biloculare. (2009): Bullockia (Bridson) Razaﬁm. Fadogia Schweinf. Carp. Calyx persistens. Seychelles. the Coffeeae alliance and the Vanguerieae alliance. Suppl. Lantz & B. with leftcontorted aestivation. and a grade consisting of the © 2013 The Linnean Society of London. Unicaulous subshrubs. For a description. Included genus: The monotypic Scyphiphora.F. Tribe Sipaneeae Bremek. Comores. 5-merous. with extensive mesocarp. Everistia S. persistens. with a reticulate. Erect shrublets. ridged. nov. occurring in tropical Asia and the western Paciﬁc. Ovarium biloculare. Calyx tubular.. (2004): Limnosipanea Hook. Included genus: Steenisia. in thyrsis axillaribus. in axillary thyrses. trib. Yunnan).Rich. 173. & B. (sub-) tropical Asia to Australia and the Paciﬁc.f. mesocarpio extenso. & B. Flowers 4(–5)-merous. Corolla funnel-shaped. Ixoroideae can be considered as being composed of two well-supported lineages. Included genera (here investigated): Afrocanthium. and Steyermarkia Standl. Madagascar. Edinburgh 10: 74 (1917) Fruticuli erecti. Corolla tubular. Stylus exsertus. granulate testa. nov. Fruits dry.W.Bremer. in terminal cymes.Bremer. Tribe Vanguerieae A. Botanical Journal of the Linnean Society. interdum uno lobo post anthesin expanso. lobis in aestivatione sinistrorsum contortis. short.Bremer. Tribe Scyphiphoreae Kainul. persistent.PHYLOGENY OF IXOROIDEAE Included genera: Hekistocarpa. in thyrsis axillaribus. Following the results of this study. Ovarium biloculare. Neblinathamnus Steyerm. Corolla rotate. Style exserted. in cymis terminalibus. CONCLUSIONS Here. Fructus schizocarpi. ovulo uno ascendenti et uno descendenti in quoque loculo. Fruits septicidal capsules..J. lobis in aestivatione sinistrorsum contortis. Corolla infundibuliformis. Seeds minute.. Canthium Lam. Lantz & Bremer (2004) and Razaﬁmandimbison et al. Keetia. with ﬁve species in Sundaland (Borneo. Type: Scyphiphora C. Eriosemopsis Robyns. we analysed the tribal relationships and delimitation in Ixoroideae using six plastid DNA regions and Bayesian and parsimony methods of phylogenetic reconstruction. Tamridaea and Virectaria. Bot. indehiscent. Mascarenes. Stylus curvatus. Flores minuti. testa reticulata granulata.. Inclusion based on Robbrecht (1988). Tribe Steenisieae Kainul. porcati. Style exserted. connatis tubumque stamineum stylum cingentem facientibus. with left-contorted aestivation. and Vangueriopsis Robyns.: 91 (1806) Frutices vel arbusculae. Fructus capsulares septicidales. Ovary bilocular.Gaertn. ovulo uno pendulo in quoque loculo. Flores 4(–5)-meri. Hutchinsonia Robyns.Reynolds & R.. ex Dum. Calyx persistent. Distribution: Central America and tropical South America. For descriptions. ovulis numerosis horizontaliter insertis. Multidentia Gilli. Calyx tubularis. with one pendulous ovule in each locule. 5-meri. Fruits schizocarpous. & Forrest. Tribe Trailliaedoxeae Kainul. Semina minuta. brevis. Fructus sicci. Psydrax. Inclusion based on Delprete & Cortés-B.T. Included genera (here investigated): Chalepophyllum Hook. lobis in aestivatione sinistrorsum contortis. Natuna Islands and Peninsular Malaysia). Calyx persistent.Hend. Maguireothamnus Steyerm. Flowers 4–5-merous. ﬂattened. Stylus exsertus. lobis indistinctis. see Robbrecht (1988) and Lantz & Bremer (2004). Temnocalyx Robyns ex Ridl. in axillary thyrses. Sabicea.. Perakanthus Robyns ex Ridl.. Ovary bilocular. complanata. Type: Steenisia Bakh. trib. Flores 4–5-meri. Peponidium...F. Webbia 8: 381 (1952) Suffrutices unicaules. tropical Africa.f. Vangueriella Verdc. Pyrostria. united and 397 forming a tube surrounding the style. Neobertiera Wernham and Sipanea Aubl. Gard.. occurring in south-western China (Sichuan. Shrubs or small trees. Ovary bilocular. see Delprete & Cortés-B. Corolla rotata. indehiscentes. Cuviera DC. Robynsia Hutch. Antherae appendicibus apicalibus prolongatis..
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Italic sequences originate from a different specimen from that indicated Species Afrocanthium lactescens (Hiern) Lantz Airosperma psychotrioides K. Huysmans S. Augusta longifolia (Spreng. Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Adansonia 2: 197–205. Airosperma vanuense S.f.Schum.) Rehder Augusta rivalis (Benth. (BR) HM119511* HM119512* HM164353* AM9498462 – AM9498422 – HM164194* HM164241* FM2047522 HM164309* FM2071182 HM119513* HM164354* EU8174136 EF2056397 FM2047532 EU8174556 FJ9053378 HM119514* FJ8719478 HM164355* HM164156* HM164157* FJ8846378 HM164195* FJ9483028 HM164242* FJ9483718 HM164310* © 2013 The Linnean Society of London.H. un nouveau genre de Rubiacées (Rondélétiées) des Seychelles. Rannala B. Dessein S. Bulletin du Jardin Botanique de l’État à Bruxelles 28: 209–281.Presl Bertiera aethiopica Hiern Voucher Luke & Luke 9045 (UPS) Nyman 569 (UPS) matK HM119502* ndhF HM164346* rbcL HM164152* rps16 HM164189* trnS-G HM164234* trnT-L-F AJ6201271 – HM164347* – – – HM164302* Sands 6819 (L) Degener & Ordonez 15542 (S) Smith 8214 (P) HM119503* – HM164348* HM164349* – – – HM164190* HM164235* – HM164303* HM164304* HM119504* AM9498452 – FM2047002 FM2047402 FM2071082 Tonkin 200 (UPS) Tange 45171 (AAU) Tange 46977 (AAU) Iverssen & Steiner 86776 (UPS) HM119505* HM119506* AJ2362823 – Y187083 HM164153* FM2047012 AF2429024 FM2047412 HM164236* AJ6201181 HM164305* HM119507* HM16435028 HM164154* AF2429034 HM164237* HM164306* HM119508* – Y118455 HM164191* HM164238* HM164307* Munzinger & McPherson 635 (MO) Mouly & Innocente 237 (P) HM119509* HM164351* HM164155* HM164192* HM164239* HM164308* HM119510* HM164352* EU8174126 HM164193* HM164240* EU8174546 Kirkbride 5295 (BR) McDowell 5017 (ETSU) Schmidt et al.) Tange Aoranthe penduliﬂora (K. 1984.) Ridl. Aleisanthia rupestris (Ridl. 2013. Smets E. Airosperma sp. 1997. Bathysa stipulata (Vell.Kirkbr. Verdcourt B. Glionnetia. 1958.n. Phylogeny of Tricalysia (Rubiaceae) and its relationships with allied genera based on plastid DNA data: resurrection of the genus 401 Empogona.H. Botanical Journal of the Linnean Society. 2009. Yang Z. Fay MF. Molecular Biology and Evolution 14: 717–724. 1672 (MO) Pirani & Bremer 4901 (SPF) Dessein s. Annals of the Missouri Botanical Garden 96: 194–213. 387–406 .P. Davis AP.) C. 173. Bulletin du Muséum National d’Histoire Naturelle.Kirkbr. including GenBank sequence accession numbers and voucher specimens for previously unpublished sequences (indicated with *). Airosperma trichotomum (Gillespie) A. Aulacocalyx jasminiﬂora Hook.Sm. Remarks on the classiﬁcation of the Rubiaceae.Schum. & Lauterb.C. De Block P.) Somers Atractocarpus balansaeanus Guillaumin Augusta austrocaledonica (Brongn.) J.Darwin Alberta magna E. Section B.Mey. APPENDIX Overview of taxon sampling.PHYLOGENY OF IXOROIDEAE Tirvengadum DD.) J. Robbrecht E. Aleisanthiopsis distantiﬂora (Merr. Tosh J.
f. Botanical Journal of the Linnean Society. conﬂuens (K.f. Cephalanthus occidentalis L.Don) Benth. Coddia rudis (E.402 K. Chalepophyllum guyanense Hook.A. Canthium coromandelicum (Burm. KAINULAINEN ET AL.) Verdc.33 HM164311* HM164312* HM119518* HM164357* – HM164197* HM164244* HM164313* HM119519* HM164358* Z6883312 HM164198* HM164245* HM164314* FJ9053408 AJ2362853 X8362713 FM2047122 FM2047562 AJ84739814 HM119520* HM164359* Z6885112 HM164199* HM164246* AJ84740114 HM119522* – AM11721411 HM164200* HM164248* HM164315* AY53837715 HM119523* FJ9053448 AJ2362883 – AJ2362893 X8362913 HM164159* Y187123 AF00403316 HM164201* FJ8846438 – HM164249* FJ9483098 AJ34695517 HM164316* FJ9483788 Z7019718 HM119524* AJ23584319 HM164361* X8363013 AJ28669520 FM2047142 HM164202* FM2047582 HM164250* AJ34696317 HM164317* Andreasen 223 (UPS) Luke 9024 (UPS) Lisowski 47195 (K) EF04421321 HM119560* HM119525* HM119526* EF04421321 HM164387* HM164362* EU14540922 EF04421321 AJ28669220 HM164160* EU14545722 EF04421321 HM164219* HM164203* AF12927223 EF04421321 HM164283* HM164251* HM164252* EF04421321 HM164333* HM164318* EU14553222 Pennington & Daza 17436 (MOL) Bremer 3810 (UPS) Andreasen 51 (UPS) Bremer 3097 (UPS) McDowell 4427 (DUKE) FJ9053478 FJ8719508 HM164161* FJ8846458 FJ9483128 FJ9483818 HM119527* HM164363* AJ28671120 HM164204* HM164253* HM164319* HM119528* AM9498502 Z6885612 FM2047162 FM2047592 FM2071212 FJ9053298 AM9498512 AM11722311 FM2047172 FM2047602 FM2071232 AY53838615 AM11734511 X8363213 FM2047182 FM2047612 FM2071242 © 2013 The Linnean Society of London. Coffea ebracteolata (Hiern) Brenan Coffea sessiliﬂora Bridson Colletoecema dewevrei (De Wild. & Alejandro Burchellia bubalina (L.) Razaﬁm. ex G.) Verdc.) Alston Catunaregam spinosa (Thunb. ex Harv. Bremeria landia (Poir.) Degreef Cremaspora triﬂora ssp.n.Petit Condaminea corymbosa (Ruiz & Pav. 256 (UPS) Bicknell 1561A (SUNIV) Andriambololonera 37 (MAU) Bremer 3129 (UPS) Sanders 1805 (FTG) Andreasen 36 (UPS) Luke 8332A (UPS) Forbes s. Bertiera longithyrsa Baker Boholia nematostylis Merr. Chimarrhis hookeri K.) Tirveng.Schum. Cubanola domingensis (Britton) Aiello Voucher Andersson et al.) E. 2013. 173.f.M.Schum. APPENDIX Continued Species Bertiera guianensis Aubl.Mey. 387–406 . 2029 (GB) Kårehed et al. (S) Sandwith 1346 (S) Delprete & Verduga 6421 (UPS) McDowell 4613 (DUKE) Bremer 3764 (UPS) matK HM119515* HM119516* HM119517* ndhF AM9498472 HM164356* AM9498482 rbcL AJ2248459 HM164158* AM11721011 rps16 AF20098310 HM164196* AM11728611 trnS-G FM2047542 HM164243* FM2047552 trnT-L-F FM2071192.) DC.) Sims Calycophyllum candidissimum (Vahl) DC. Cinchona pubescens Vahl. Coptosperma supra-axillare (Hemsl. Coffea arabica L. Crossopteryx febrifuga (Afzel.
macrophylla (Ducke) Steyerm.St. Genipa americana L. no. & Krause Ferdinandusa speciosa Pohl Feretia apodanthera Delile Fernelia buxifolia Lam. K. 4302 (UPS) De Block 27 (BR) Bremer & Bremer 3799 (UPS) Malme 2442 (UPS) Luke 8385 (UPS) Nat.f. Fadogia tetraquetra K. & A. Empogona coriacea (Sond. Hyperacanthus grevei Rakotonas. WAG) Liesner 8531 (MO) matK HM119529* ndhF – rbcL EU8174166 rps16 EF2056407 trnS-G HM164254* trnT-L-F EF2056317 FJ9053248 FJ8719438 HM164162* FJ8846278 FJ9482918 FJ9483608 FJ9053498 FJ8719528 HM164163* FJ8846478 FJ9483148 FJ9483838 HM119531* HM164365* AJ28670920 HM164205* HM164256* HM164320* FJ9053608 HM119574* AJ2362943 HM164401* Y187153 HM164184* FM2047192 HM164228* FM2047622 HM164295* FM2071252 HM164340* HM119532* HM119533* HM164366* HM164367* Z6883512 AM11722511 HM164206* HM164207* HM164257* HM164258* AJ84739914 AJ6201391 HM119534* HM119535* HM119536* EU14541222 HM164368* HM164369* AM11722611 HM164164* AJ28670420 FJ8846578 HM164208* AF2448924 FJ9483278 HM164259* HM164260* EU14553422 HM164321* EU14554022 HM119537* AM9498522 AJ31844624 AJ32007724 FM2047632 FM2071262 AJ42932225 AJ01198426 L1439727 AJ43103325 – AJ43090825 HM119538* HM164370* Z6883912 HM164209* HM164261* HM164322* HM569720* HM119539* AY53838915 HM119540* HM119541* HM53621728 HM164371 FJ8719428 HM164372* HM164373* HM53622328 HM53622928 HM569721* – AY53848515 Y118495 AF33236629 EU8174396 AF2429644 HM164210* AF33236729 HM164262* FJ9482898 HM164263* HM164264* HM53623528 EU8174596 FJ9483588. Botanical Journal of the Linnean Society. 2013.) Tosh & Robbr. 173. Gardenia hansemannii K. HBVsub RR-420 (WU. UPS) Beaver 17 (S) Larsen & Larsen 33451 (P) Persson 141 (GB) McPherson 16188A (MO) Leuwenberg 6393 (BR. & Krause) Steyerm.-Hil. Gelsemium sempervirens (L.Schum.Taylor Hekistocarpa minutiﬂora Hook. Hippotis triﬂora Ruiz & Pav.) J.f.Davis 403 Voucher Mouly & Innocente 228 (P) Prance et al. Bot. Gard.n. Meise. Greenea oblonga Craib Guettarda speciosa L. 16199 (S) Zarucchi & Echeverry 4780 (MO) cult. 19940025-26 Drozd & Molem 1998-11-13 Bremer 3026 (UPS) Kiehn. Euclinia longiﬂora Salisb. Henriquezia nitida var. Duperrea pavettifolia (Kurz) Pit.) G. Emmenopterys henryi Oliv. Glionnetia sericea (Baker) Tirveng. Heinsia crinita (Afzel.P.PHYLOGENY OF IXOROIDEAE APPENDIX Continued Species Cyclophyllum deplanchei Hook. Dendrosipanea spigelioides Ducke Dioicodendron dioicum (K.34 HM164323* HM164324* – HM164374* – HM164211* – HM164325* Ståhl 2660 (GB) FJ9053658 FJ8719568 HM164375* HM164165* HM164166* FJ8846598 HM164212* FJ9483298 HM164265* FJ9483978 HM164326* Razaﬁmandimbison HM119542* 547 (UPS) © 2013 The Linnean Society of London. (UPS) Bremer et al.Schum. Bergius Botanic Garden Robbrecht s. 387–406 .Schum.
Bremer Ixora novoguineensis Mouly & B.Hallé) Mouly & B.n.) Benth. 387–406 .) Kurz Ixora borboniae Mouly & B.) F.404 K.Sm.) A.Muell. Botanical Journal of the Linnean Society. 2013. Ixora ferrea (Jacq. Ixora margaretae (N. Ophiorrhiza mungos L. Mitriostigma axillare Hochst.Bremer Ixora coccinea L.) Tirveng.) Mouly & B. APPENDIX Continued Species Hypobathrum racemosum (Roxb. Mussaenda arcuata Poir. Multidentia concrescens (Bullock) Bridson & Verdc. 173. Keetia gueinzii (Sond.) Bridson Landiopsis capuronii Capuron ex Bosser Logania vaginalis (Labill.C.) Ridsdale Kailarsenia tentaculata (Hook. Mussaenda erythrophylla Schumach. Luculia gratissima (Wall. & Thonn.f. 4349 (UPS) Gautier 4533 (MO) HM119546* HM119547* HM53621328 HM164378* HM53621928 HM53622528 HM164268* HM164168* HM164213* HM164269* HM53623128 HM164327* HM119548* HM119549* HM164379* HM164380* HM164169* HM164170* HM164214* HM164215* HM164270* HM164271* AJ6201431 HM164328* Bremer 3013 (UPS) CT 870064 Rova & Gustavsson 2429 (GB) Bremer 2705 (UPS) Williams 6861 (S) Bidgood et al. Molopanthera paniculata Turcz. Voucher Ridsdale 81 matK HM119543* ndhF AM9498532 rbcL AJ28670520 rps16 AM11731811 trnS-G HM164266* trnT-L-F FM2071272 Friedmann 3049 (P) Bremer 2719 (UPS) Taylor 11693 (MO) Mouly & Innocente 222 (P) Drozd & Molem 1998-11-13 HM119552* HM164383* HM164173* FJ1506856 HM164275* FJ1506096 HM119544* HM119545* HM119521* HM164376* HM164377* HM164360* HM164167* EU8174226 EU8174156 EF2056417 EF2056427 EU8174366 FM2047642 HM164267* HM164247* EU8174646 EU8174656 EU8174566 HM119581* HM164406* AJ31845924 AJ32009024 HM164300* EU8174766 Lesouef 31 (TAN) HM119530* HM164364* EU8174176 EU8174376 HM164255* EU8174576 K. Neobertiera gracilis Wernh.Bremer Ixora trilocularis (Balf. 845 (K) AJ42932425 AJ42932525 FJ9053698 AJ23583719 AJ01198726 FJ8719598 Z6882612 AM11724311 HM164171* AJ43103525 AJ43103625 AF2429794 HM164272* FM2047652 FJ9483328 AJ43091025 AJ43091125 FJ9484018 HM119550* – – HM164381* HM164382* – X8365013 HM164172* – HM164216* AF2429814 – HM164273* – HM164274* HM164329* FJ948361* AJ6201501 McPherson 16213 (MO) Gillis 10838 (FTG) HM119551* FJ9053268 AJ2363013 AJ1308363 Y118545 X8365213 FM2047212 FJ8846288 FM2047672 FJ9482928 FM2071282 AJ6201161 Bremer 3001 (UPS) de Granville 2888 (NY) Bremer 3301 (UPS) AY53840715 – AY53840815 EU14541022 – AJ1308383 X8365313 – X8365613 AJ32008024 AF2429844 AF00406416 HM164276* – HM164277* AJ34695817 AF15267930 DQ66215131 © 2013 The Linnean Society of London. Nauclea orientalis (L. KAINULAINEN ET AL. Tan s. S.f.) L. Larsen 41627 (AAU) Bremer et al.) Sweet Mastixiodendron ﬂavidum (Seem.Bremer Jackiopsis ornata (Wall.
1941 (GB) Sabicea diversifolia Bremer et al.PHYLOGENY OF IXOROIDEAE APPENDIX Continued Species Oxyanthus speciosus DC. Paragenipa lancifolia (Bojer ex Baker) Tirveng.) K. Botanic Garden Pseudomussaenda Nissen s.X. Pavetta indica L. 173. (UPS) ﬂava Verdc.1–145 Retiniphyllum Wurdack & pilosum (Spruce Adderley 43270 ex Benth. 2013. Rothmannia Bremer et al.n. 3762 (UPS) & Zeyh.x. 4018-B18 (UPS) Schizomussaenda Puff 961116-1/1 henryi (Hutch.36 HM119566* HM164393* HM164177* HM164222* HM164287* HM164335* HM119567* FJ9053858 HM164394* AJ2363103 AM11726611 Y187163 AM11734011 FM2047312 HM164288* FM2047772 AM11738411 FM2071382 – – HM164178* HM164223* HM164289* AJ6201751 – AY53842015 HM119568* HM119569* HM164397* EU14541622 EU14541522 HM164395* HM164180* AY53850815 EU14545922 AM11727311 HM164225* AF00407916 EU14549422 HM164224* HM164292* FJ9482938 HM164290* HM164291* HM164337* FJ9483628. Andreasen 3504 (UPS) Rosenbergiodendron Jansen-Jacobs densiﬂorum (K. 3977 (GB) Schum. Aubl. Pers. Rondeletia odorata Bremer & Jacq. & Robbr Pavetta abyssinica Fresen. 2236 horridum Arènes (K) Pinckneya bracteata Massey s. 387–406 . & (UPS) Schult. Psydrax obovata Bremer & Bremer (Klotzsch ex Eckl. Wieringa 3591 Beauv.) Delprete Rytigynia van den Berghen senegalensis 8746 (BR) Blume Sabicea africana (P. Posoqueria latifolia Andreasen 90 (Rudge) Roem. 15F (Bartram) Raf.Zhang HM119558* HM119559* HM119561* HM164386* AM9498562 HM164388* HM164175* Y118555 HM164176* HM164218* FM2047292 HM164220* HM164282* FM2047752 HM164284* HM164332* FM2071362 AJ6201611 HM119562* HM119563* – HM164389* HM164390* HM164392* AM11726211 Z6883212 AF33165432 AM11733811 HM164221* AF00407616 HM164285* HM164286* FM2047762 AJ6201681 HM164334* FM2071372 – AJ23584519 Y118575 AF2430104 FJ9482908 FJ9483598. 405 Voucher Bremer 4348 (S) Persson 156 (GB) matK HM119554* HM119555* ndhF HM164384* HM164385* rbcL AM11725211 AJ28670720 rps16 AM11733011 AF00406616 trnS-G HM164278* HM164279* trnT-L-F AM11737511 HM164330*35 De Block 6 (BR) HM119556* HM119557* – FJ9053778 FJ9053788 FJ9053258 AM9498542 – – AJ1308393 FJ8719648 AM9498552 Z6886312 – – X8366113 HM164174* Z6885012 FM2047262 HM164217* – FJ8846688 FJ8846708 FM2047282 FM2047722 HM164280* HM164281* FJ9483398 FJ9483418 FM2047742 FM2071332 HM164331* AJ6201531 FJ9484088 FJ9484108 FM2071352 Andreasen 202 (UPS) Peponidium Labat et al. Posoqueria cult.Deng & D.n.) Bridson Pyrostria hystrix Bremer & Bremer (Bremek. Pogonopus speciosus Meier 2548 (GB) (Jacq.) Bridson 3791 (UPS) Randia aculeata L.) (WU) X. (S) Rustia Delprete 6378 thibaudioides (UPS) (H.F.) Fagerl.G. (S) Arg.37 AJ84739614 AJ84738314 © 2013 The Linnean Society of London. F.Schum. Bergius longiﬂora Aubl. Botanical Journal of the Linnean Society.Karst.) Hepper (WAG) Sabicea aspera Andersson et al.) Müll. 4346 capensis Thunb.
f.Sm. APPENDIX Continued Species Scyphiphora hydrophyllacea C. 26Oxelman. Backlund & Bremer (1999).) DC. 13Bremer et al. Oxelman & Bremer (2000). 3Bremer et al. 30Rova et al. 34with AF152725. 9Andreasen.406 K. (1993). © 2013 The Linnean Society of London.) Verdc. 8Kainulainen et al. 22Rydin et al.W. (2001).Gaertn. (2002). data).) Steyerm. 32L. (2009). (2010). 99 (S) Bremer 3361 (UPS) Rova et al. 29Dessein et al. (2002). 12Andreasen & Bremer (1996). 6Mouly et al. 10192 (UPS) Chung 1403 (S) Rechinger 183 (S) HM119570* AM9498582 AM9498432 FM2047372 FM2047832 FM2071442 HM119571* HM119573* AM9498592 HM16440028 HM164181* FM2047382 FM2047842 FM2071452 HM16433928 HM16418328 HM16422728 HM164294* HM119575* AJ1308403 X8367013 HM164229* FM2047852 AJ6201841 HM119576* HM119577* HM119578* HM164402* HM164403* HM164404* HM164185* HM164186* HM164187* HM164230* HM164231* AF2430364 HM164296* HM164297* HM164298* HM164341* HM164342* HM164343*39 Ridsdale 2179 HM119579* HM164405* HM164188* HM164232* HM164299* HM164344* Parker 3227 (S) HM119580* AM9498602 FM2076492 FM2047392 FM2047862 FM2071472 Adames 606 (UPS) HM119582* HM164407* Y118615 HM164233* HM164301* HM164345* Published sequences: 1Lantz & Bremer (2004). 27Olmstead et al. 2369 (GB) Boufford et al. Andersson (unpubl. 36with AF152741. 17Razaﬁmandimbison & Bremer (2002). 31Backlund. 35041 (MO) Sanders 1798. E. 38with AF152675.38 – EU14541422 EU14545822 EU14549222 – HM164336* FJ9053288 HM164396* AM11727911 FM2047352 FM2047812 FM2071422 – HM164398* Y118605 FM2047362 FM2047822 FM2071432 Abdalla et al. Baldwin & Bremer (1999). Wendlandia arabica Deﬂers Wendlandia formosana Cowan Wendlandia ligustroides (Boiss. 23Piesschaert et al. 16Andersson & Rova (1999). 7Mouly et al. (2008). Sipanea hispida Benth. 2013. 387–406 . (1996). (2000). Voucher Bremer et al.Gmel.) DC. 24Novotny et al.F. (2007). (2007). & Bridson Tocoyena pittieri (Standl. & Forrest Vangueria madagascariensis J. Combined sequences: 33with AF152670. (1999). 4J. 2Kainulainen et al. 37with AY538475.) Cham. (2011). (2002). biﬂora (L. 35with AF152672. (1995).) Bremek.f. Sipanea aff.) Thulin & B.f. 28 Razaﬁmandimbison et al. Rova (unpubl. Virectaria multiﬂora (Sm. Simira cordifolia (Hook. 19Backlund.) Blakelock Wendlandia paniculata (Roxb. 20Andreasen & Bremer (2000). & Schltdl. KAINULAINEN ET AL. (2009a). Wendlandia tinctoria (Roxb. 5Bremer & Thulin (1998). 25Bremer et al. Trailliaedoxa gracilis W. 11Bremer & Eriksson (2009). & Hohen. data). Bremer & Thulin (2007). 39with AF152661. 21Samson et al.) Standl. 18Endress et al. Botanical Journal of the Linnean Society. 173. 2005 (GB) Irwin et al. ex Wernham Steenisia pleurocarpa (Airy Shaw) Bakh. Bremer Tennantia sennii (Chiov. Tamridaea capsulifera (Balf.F.f. 34756 (UPS) Puff BF 990619-1/4 (WU) Thulin & Gifri 8663 (UPS) matK FJ9053278 ndhF AJ2363113 rbcL Y187173 rps16 EU8174506 trnS-G FM2047792 trnT-L-F EU8174756 FJ9053888 AY53842115 FJ8719708 EU14541322 HM164179* AY53850915 FJ8846778 AF00408516 FJ9483508 FM2047802 FJ9484198 FM2071412. H. 10Persson (2000). 96/166 (P) Rova et al. (2005). 15Andersson & Antonelli (2005). 14Alejandro et al. #62146 (FTG) Thulin et al.
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