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Phylogenetic Position of the Genus Ferula (Apiaceae) and Its Placement in Tribe Scandiceae As Inferred from Nrdna ITS Sequence Variation

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Phylogenetic Position of the Genus Ferula (Apiaceae) and Its Placement in Tribe Scandiceae As Inferred from Nrdna ITS Sequence Variation Plant Syst Evol DOI 10.1007/s00606-008-0022-2 ORIGINAL ARTICLE Phylogenetic position of the genus Ferula (Apiaceae) and its placement in tribe Scandiceae as inferred from nrDNA ITS sequence variation Renata Kurzyna-Młynik Æ Alexei A. Oskolski Æ Stephen R. Downie Æ Rafał Kopacz Æ Aneta Wojewo´dzka Æ Krzysztof Spalik Received: 14 June 2007 / Accepted: 28 January 2008 Ó Springer-Verlag 2008 Abstract Recent molecular systematic investigations accessions of Ferula misplaced in the apioid superclade suggested that Ferula, an umbellifer genus of about 170 represent a species of Silaum. species, is polyphyletic, with its members placed in the apioid superclade and within tribe Scandiceae. We ana- Keywords Apiaceae Á Ferula Á Ferulinae Á nrDNA ITS Á lyzed ITS sequence variation from 134 accessions of Phylogeny Á Scandiceae Á Umbelliferae Apiaceae, including 83 accessions (74 species) of Ferula to ascertain the phylogenetic position of the genus within the family. Phylogenetic analyses of these data using maxi- Introduction mum parsimony, Bayesian, and neighbor-joining methods support the monophyly of Ferula upon the addition of The genus Ferula L. includes about 170 species extending Dorema and Leutea (as Ferula sensu lato) and its place- from central Asia westward throughout the Mediterranean ment in tribe Scandiceae. Ferula sensu is closely allied region to northern Africa (Pimenov and Leonov 1993). Many with other major lineages of Scandiceae, corresponding to species have been known since antiquity as sources of aro- subtribes Scandicinae, Daucinae, and Torilidinae. There- matic resins used in traditional medicine. These include fore, we recognize the Ferula clade as subtribe Ferulinae. asafoetida (obtained from F. assa-foetida, F. aliacea Boiss., Another addition to tribe Scandiceae is a clade composed F. foetida, and F. narthex Boiss.; authorities for species used of genera Glaucosciadium and Mozaffariania. The three in this study are given in the ‘‘Appendix’’), sagapenum (F. persica Willd., F. szowitsiana), galbanum (F. gummosa), sumbul (F. moschata), and African ammoniacum (F. tingi- tana, F. communis) (Korovin 1959). Crowned with a pine R. Kurzyna-Młynik Á R. Kopacz Á A. Wojewo´dzka Á cone and covered with ivy vines and leaves, a dried stalk of K. Spalik (&) Department of Plant Systematics and Geography, Ferula made the ancient thyrsus, a walking stick and an Faculty of Biology, University of Warsaw, attribute of Dionysus and his followers Satyrs and Maenads. Aleje Ujazdowskie 4, 00-478 Warszawa, Poland A plain stalk also served schoolmasters for inflicting cor- e-mail: [email protected] poral punishment on pupils (Beazley 1933). There are also A. A. Oskolski speculations whether the famous spice and medicine of Botanical Museum, Komarov Botanical Institute, ancient Greece and Rome, silphium, came from a member of Prof. Popov str. 2, 197376 St Petersburg, Russia this genus. This plant, gathered from the wild in the coastal region of Cyrenaica (present Libya), went extinct around first S. R. Downie Department of Plant Biology, century BCE, probably as a result of overexploitation and University of Illinois at Urbana-Champaign, grazing (Andrews 1941). Urbana, Illinois 61801, USA Despite its large number of species, the genus is usually recognized as monophyletic, because its members are A. Wojewo´dzka Botanic Garden of University of Warsaw, Aleje Ujazdowskie 4, similar in habit and morphology. These robust, tall peren- 00-478 Warszawa, Poland nials or biennials are characterized by prominent taproots, 123 R. Kurzyna-Młynik et al. stout stems, finely divided leaves with large inflated that Ferula is distinct from all other peucedanoid genera sheaths, and dorsally compressed fruits with plane com- they included in their study. missural faces. However, there is also considerable Several large umbellifer genera are ‘‘dustbin’’ taxa variation in leaf division and indumentum, flowers and encompassing species that do not fit elsewhere. Large inflorescences, and fruit anatomy resulting in the recogni- genera with more than 20 species each comprise some 60% tion of numerous and often hardly discernible taxa. Basal of the total number of umbellifer species (Spalik et al. leaves and mature fruits are important for correct identifi- 2001a). These include such genera like Conioselinum cation; the former, however, are usually dried up before the Hoffm., Cymopterus Raf., Heracleum L., Ligusticum L., latter are fully ripe. Because of the large size of these Peucedanum, and Seseli L., which have each already been plants, only its lateral branches and lateral divisions of its shown to be polyphyletic (Katz-Downie et al. 1999; basal leaves are usually preserved, thus making the iden- Downie et al. 2000b, 2002). Therefore, the polyphyly of tification of herbarium specimens difficult. With the large genus Ferula as suggested by molecular data is experience, most of the species can be identified from not a surprise. However, in contrast to the aforementioned flowering material (Chamberlain and Rechinger 1987). genera, Ferula has long been regarded as a natural taxon. However, the delimitation of species requires examination Moreover, despite the considerable phylogenetic distance of complete specimens with roots, stem bases, basal leaves, between the two Ferula clades as suggested by previous inflorescence, flowers, and ripe fruits, and should be based molecular studies, we could not find any morphological on observations of living plants (Korovin 1947). It is not character distinguishing these groups (A. Wojewo´dzka, surprising, therefore, that both the infrageneric classifica- University of Warsaw Botanic Garden, unpublished data). tion of Ferula and its phylogenetic position remain The most comprehensive infrageneric classification of disputed. Ferula is that proposed by Korovin (1939, 1940, 1947); Ferula is traditionally classified in tribe Peucedaneae subsequently, it was modified for the Flora of the USSR subtribe Ferulinae (Drude 1897–1898; Pimenov and Leo- (Korovin 1951). Korovin recognized six subgenera and nov 1993). Similar to most traditionally circumscribed, eight sections, with some of these sections being divided higher level taxa within Apiaceae, molecular systematic into series or ‘‘grex’’ categories (Table 1). This classifica- studies have revealed that tribe Peucedaneae and its sub- tion was rarely adopted in extenso. In their revision of tribes are each polyphyletic (Downie and Katz-Downie Ferula for the Kazakhstan flora, Safina and Pimenov 1996; Plunkett et al. 1996). Many former members of (1984) rejected Korovin’s subgenera and recognized 12 Peucedaneae, including Peucedanum L. sensu lato, are now sections instead. Chamberlain and Rechinger (1987), in classified in tribe Selineae (Spalik et al. 2004). Phylo- their revision of Ferula for Flora Iranica, retained only genetic analyses of both nuclear ribosomal DNA (nrDNA) Korovin’s subgenera, but refrained from referring four internal transcribed spacer (ITS) and chloroplast DNA newly described species to any of them. Pimenov et al. (cpDNA) rps16 intron sequences suggest that Ferula is (1978) carried out a phenetic cluster analysis of 90 species also polyphyletic. Of its eight species considered in pre- of Ferula using 33 morphological, life history, and vious molecular studies, three (F. communis, F. tingitana, phytochemical characters. Their results were incongruent and F. assa-foetida) form a clade with ‘‘Thysselinum pa- with the classification of Korovin. lustre’’ and Cenolophium denudatum (Fisch. ex Hornem.) Korovin (1947) argued that fruit anatomy was of little Tutin within the apioid superclade (Downie et al. 1998; value for the classification of Ferula; so, he used mostly Katz-Downie et al. 1999; Downie et al. 2000c), whereas characters of leaves and flowers to delimit infrageneric the remaining species ally, surprisingly, with members of taxa. In contrast, Safina and Pimenov (1983, 1984, 1990) tribe Scandiceae (Valiejo-Roman et al. 1998; Downie et al. stressed the importance of fruit characters for circum- 2000c; Lee and Downie 2000). The accession of ‘‘Thys- scribing sections and inferring phylogenetic relationships. selinum palustre’’ used in these analyses was subsequently In their revision of Ferula for Kazakhstan, Safina and revealed to represent an unidentified umbellifer species Pimenov (1984) described nine basic fruit types, with most rather than T. palustre (L.) Hoffm.; the latter and its sections they recognized being monomorphic with respect congeners are members of tribe Selineae (Spalik et al. to fruit anatomy. In studies of Korovin’s subgenera Peu- 2004). The affinity of Ferula with Scandiceae does not cedanoides (Safina and Pimenov 1983) and Ferula (Safina receive support from any line of evidence other than DNA and Pimenov 1990), they provided evidence suggesting sequences. However, the distant position of Ferula from that these subgenera are highly heterogeneous with respect other member genera of traditionally delimited Peuceda- to fruit anatomy, with some of their respective members neae is confirmed by serological data. The more similar to those of other subgenera. While demon- immunochemical studies of Shneyer et al. (1995, 2003), strating that the classification system of Korovin is while demonstrating the homogeneity of the genus, showed artificial, the carpological studies of Safina and Pimenov 123 Phylogenetic position of the genus Ferula (Apiaceae) and its placement Table 1 Infrageneric classification of Ferula as proposed by Korovin (1947), with later additions and synonymy
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