Molecular phylogeny and taxonomy of Tanacetum L. (Compositae, Anthemideae) inferred from nrDNA ITS and cpDNA trnH–psbA sequence variation

Abstract

The genus Tanacetum L. consists of around 160 species of the Compositae-Anthemideae. It holds a crucial position for understanding the phylogeny of the tribe and its subtribal and generic classification. The present study focuses on the phylogenetic relationships of the species and aims at a discussion of the infrageneric classification and boundaries of the genus. Sequence information from a nuclear [nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS)] and a chloroplast marker [chloroplast DNA (cpDNA) trnH–psbA] was used to infer the phylogeny of Tanacetum and many representatives of closely related genera. Bayesian inference methods were used for the phylogenetic reconstructions based on a combined dataset including both sequence and indel information. Contrasting the high morphological diversity in the genus, sequence divergence among Tanacetum representatives included was found to be very low, leading to unresolved phylogenetic relationships within the genus. Nevertheless, the generic separation of Tanacetum from other members of subtribe Anthemidinae (i.e., Anthemis, Archanthemis, Cota, Nananthea, and Tripleurospermum) emerges, while other, presently accepted genera are found nested in Tanacetum (i.e., Gonospermum, Lugoa, and Xylanthemum). Finally, the phylogenetic independence of the SW European T. microphyllum from the rest of Tanacetum and the other genera of Anthemidinae is found to receive strong support and is also backed by its morphological uniqueness. The new genus Vogtia Oberpr. et Sonboli is described to accommodate Tanacetum microphyllum and the closely related species T. annuum. The sinking of Gonospermum, Lugoa, and Xylanthemum into a broadly circumscribed genus Tanacetum is proposed until more stable phylogenetic reconstructions based on more and more variable molecular markers are possible. Concerning the infrageneric classification of Tanacetum, the phylogeny does not support the separation of the white- and red-rayed species (the former genus Pyrethrum) from the discoid, disciform, or yellow-rayed ones (i.e., Tanacetum in the strict sense) at any infrageneric rank. The hypothesis by Tzvelev (1961) that the yellow-rayed representatives may have evolved from disciform ancestors receives little support.

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Acknowledgments

The authors gratefully acknowledge the curators of herbaria B, G, IRAN, M, MSB, MPH, S, TARI, and W for providing leaf material for DNA analysis. We would like to express our thanks to Dr. R. M. Lo Presti (Regensburg) for permission to include a number of cpDNA sequences of Anthemis and Cota in this study. Some of the nrDNA sequences were also established during a student training course by Birgit Blaul (Regensburg). Laboratory technical assistance of Miss K. Naderi (Teheran) and Mr. P. Hummel (Regensburg) and nomenclatural advice of Prof. Dr. W. Greuter (Berlin) is highly appreciated. This research was partly supported by the German Academic Exchange Service (DAAD) and the Shahid Beheshti University Research Council to A.S. and by the SYNTHESYS project of the EU to C.O. (SE-TAF-1084, AT-TAF-1731).

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Correspondence to Ali Sonboli or Christoph Oberprieler.

Appendix

Appendix

List of taxa and sources of plant material used for the current molecular study [taxa, source and voucher data, GenBank accession numbers (ITS, and trnH–psbA)]. The two accession numbers for nrDNA ITS of some taxa represent ITS1 and ITS2 regions, respectively.

Ajania tibetica (Hook. f. et Thomson) Tzvel., Pakistan, Polunin 6306 (B), AB683256/AB683257, AB683343. Achillea biebersteinii C. Afan., Oberprieler (2004b), AJ864573/AJ864593, AB683344. A. filipendulina Lam., Oberprieler (2004b), AJ864574/AJ864594, AB683345. A. vermicularis Trin., Oberprieler (2004b), AJ864576/AJ864596, AB683346. Anacyclus clavatus (Desf.) Pers., Oberprieler (2004a), AJ748762/AJ748763, AB683347. A. homogamos (Maire) Humphries, Oberprieler (2004a), AJ748764/AJ748765, AB683348. Anthemis ammophila Boiss. et Helder., Lo Presti and Oberprieler (2009), FM957716, FR689847. A. arvensis L., Oberprieler (2001), AJ312777/AJ312806, FR689795. A. boveana Gay, Lo Presti and Oberprieler (2009), FM957665, FR689799. A. brachystephana Bornm. et Gauba, Lo Presti and Oberprieler (2009), FM957666, FR689800. A. bushehrica Iranshahr, Lo Presti and Oberprieler (2009), FM957721, FR689851. A. cretica L., Lo Presti and Oberprieler (2009), FM957778, FR689805. A. davisii Yavin, Lo Presti and Oberprieler (2009), FM957725, FR689855. A. filicaulis (Boiss. et Helder.) Greuter, Lo Presti and Oberprieler (2009), FM957728, FR689858. A. gharbensis Oberpr., Oberprieler (2001), AJ312778/AJ312807, FR689784. A. hebronica Boiss. et Kotschy, Lo Presti and Oberprieler (2009), FM957674, FR689806. A. hyalina DC., Oberprieler (2001), AJ312779/AJ312808, FR689807. A. kotschyana Boiss., Lo Presti and Oberprieler (2009), FM957676, FR689808. A. maritima L., Oberprieler (2001), AJ312788/AJ312817, FR689772. A. pedunculata Desf., Oberprieler (2001), AJ312791/AJ312820, FR689774. A. rascheyana Boiss., Lo Presti and Oberprieler (2009), FM957702, FR689832. A. rigida Boiss. et Heldr., Oberprieler (2001), AJ312782/AJ312811, FR689777. A. schizostephana Boiss. et Hausskn., Lo Presti and Oberprieler (2009), FM957753, FR689879. A. secundiramea Biv., Lo Presti and Oberprieler (2009), FM957688, FR689776. A. tricolor Boiss., Lo Presti and Oberprieler (2009), FM957760, FR689886. A. tricornis Eig, Lo Presti and Oberprieler (2009), FM957761, FR689887. A. zaianica Oberpr., Oberprieler (2001), AJ312784/AJ312813, FR689783. A. zoharyana Eig., Lo Presti and Oberprieler (2009), FM957714, FR689844. Archanthemis calcarea (Soson.) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), Lo Presti et al. (2010), FM957769, FR689801. A. fruticulosa (M. Bieb.) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), Lo Presti et al. (2010), FM957772, FR689897. A. marschaliana (Willd.) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), Lo Presti et al. (2010), FM957698, FR689828. A. trotzkiana (Claus ex Bunge) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), Lo Presti et al. (2010), FM957684, FR689815. Artemisia vulgaris L., Oberprieler and Vogt (2000), AJ3296389/AJ3296424, AB683349. Artemisiella stracheyi (Clarke) Ghafoor, Oberprieler et al. (2007), AM774421, AB683350. Cota austriaca (Jacq.) Sch. Bip., Lo Presti and Oberprieler (2009), FM957663, FR689797. C. dipsacea (Bornm.) Oberpr. et Greuter, Lo Presti and Oberprieler (2009), FM957727, FR689857. C. dumetorum (Sosn.) J. Holub, Lo Presti and Oberprieler (2009), FM957672, AB683351. C. macroglossa (Somm. et Lev.) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), FM957787, FR689909. C. mazandaranica (Iranshahr) Lo Presti et Oberpr., Lo Presti and Oberprieler (2009), FM957741, FR689868. C. melanoloma (Trautv.) Holub, Lo Presti and Oberprieler (2009), FM957743, FR689870. C. oxylepis Boiss., Lo Presti and Oberprieler (2009), FM957782, FR689905. C. tinctoria J. Gay, Lo Presti and Oberprieler (2009), FM957758, FR689884. Cymbopappus adenosolen (Harv.) B. Nord., Himmelreich et al. (2008), AM774449, AB683352. Gonospermum fruticosum (Smith ex Link) Less., Sonboli and Oberprieler (2010), FN827335/FN827336, AB683353. Handelia trichophylla (Schrenk) Heimerl, Oberprieler et al. (2007), AM774422, AB683354. Heliocauta atlantica (Litard. et Maire) Humphries, Oberprieler (2004a), AJ748782/AJ748783, AB683355. Hippolytia dolichophylla (Kitam.) Bremer et Humphries, Oberprieler (2004a), AJ748784/AJ748785, AB683356. Leucocyclus formosus Boiss., Oberprieler (2004b), AJ864578/AJ864598, AB683357. Lugoa revoluta (C. Smith ex Link) DC., Sonboli and Oberprieler (2010), FN827337/FN827338, AB683358. Matricaria matricarioides Porter ex Britton, Oberprieler and Vogt (2000), AJ3296412/AJ3296447, AB683359. Microcephala lamellata (Bunge) Pobed., Gemeinholzer et al. (2006)/Turkmenistan, Belianiana et Sofeikova 13688 (B), AJ880341/AB683259, AB683360. Nananthea perpusilla (Loisel.) DC., Oberprieler (2004b), AJ864579/AJ864599, AB683361. Oncosiphon grandiflorum (Thunb.) Källersjö, Himmelreich et al. (2008), AM774465, AB683362. Osmitopsis asteriscoides (P. Bergius) Less., Himmelreich et al. (2008), AM774466, AB683363. Otanthus maritimus (L.) Hoffmanns. et Link, Oberprieler and Vogt (2000), AJ3296385/AJ3296420, AB683364. Phaeostigma salicifolium (Mattf.) Muldashev, Oberprieler et al. (2007), AM774423, AB683365. Phymaspermum leptophyllum (DC.) Jackson, Himmelreich et al. (2008), AM774467, AB683366. Picrothamnus desertorum Nutt., Oberprieler et al. (2007), AM774424, AB683367. Pseudohandelia umbellifera (Boiss.) Tzvel., Gemeinholzer et al. (2006)/Himmelreich et al. (2008), AJ880330/AM774468, AB683368. Richteria pyrethroides Kar. et Kir., Oberprieler et al. (2007), AM774425, AB683369. R. tianschanica (H. Kraschen.) Sonboli et Oberpr., Oberprieler et al. (2007), AM774430, AB683370. Sclerorhachis platyrhachis (Boiss.) Podl., Oberprieler et al. (2007), AM774426, AB683371. Tanacetopsis eriobasis (Rech. f.) Koval., Oberprieler et al. (2007), AM774427, AB683372. Tanacetum abrotanifolium (L.) Druce, Iran, Assadi et Olfat 68865 (TARI), AB683260, AB683373. T. abrotanifolium (L.) Druce, Oberprieler (2004b), AJ864582/AJ864602, AB683374. T. achilleifolium (M. Bieb.) Sch.-Bip., Kazakhstan, Karis 609 (S), AB683261/AB683262, AB683375. T. alyssifolium (Bornm.) Grierson, Turkey, Nydegger 46409 (MSB), AB683263/AB683264, AB683376. T. argenteum subsp. canum (Koch.) Grierson, Turkey, Nydegger 46856 (B), AB683265, AB683377. T. argenteum subsp. flabellifolium (Boiss. et Heldr.) Grierson, Celik 1976 (HUB), AB683266, AB683378. T. armenum (DC.) Sch.-Bip., Turkey, Bozakman et Fitz 826, (W, 1972-03416), AB683267, AB683379. T. aucherianum (DC.) Sch.-Bip., Turkey, (HUB), AB683268, AB683380. T. bachtiaricum Mozaff., Iran, Sonboli et al. 1174 (MPH), AB683269, AB683381. T. balsamita L., Iran, Sonboli et al. 1126 (MPH), AB683270, AB683382. T. balsamita L., Oberprieler (2004b), AJ864583/AJ864603, AB683383. T. bamianicum Podl., Afghanistan, Rechinger 18238 (B), AB683271, AB683384. T. bipinnatum (L.) Sch.-Bip., Alaska, Viereck 7431 (S), AB683272/AB683273, AB683385. T. budjnurdense (Rech. f.) Tzvel., Iran, Memariani 38119 (FUMH), AB683274, AB683386. T. canescens DC., Oberprieler (2004b), AJ864584/AJ864604. T. chiliophyllum (Fisch. et C. A. Mey.) Sch.-Bip., var. chiliophyllum, Iran, Sonboli et al. 1124 (MPH), AB683275, AB683387. T. chiliophyllum (Fisch. et C. A. Mey.) Sch.-Bip., Oberprieler (2004b), AJ864585/AJ864605, AB683388. T. chiliophyllum var. oligocephalum (DC.) Sosn., Iran, Sonboli et al. 1216 (MPH), AB683276, AB683389. T. cinerariifolium (Trev.) Sch.-Bip., Iran, Sonboli 990 (MPH), AB683277, AB683390. T. coccineum (Willd.) Grierson, Sonboli and Oberprieler (2010), FN823081, AB683391. T. corymbosum (L.) Sch.-Bip., Oberprieler and Vogt (2000), AJ3296414/AJ3296449, AB683392, T. demetrii Manden., Georgia, Merello et al. s.n. (W, 2001-10597), AB683278, AB683393. T. densum (Lab.) Sch.- Bip., HB Jena, Oberprieler 9765 (herb. C. Oberprieler), AB683279/AB683280, AB683394. T. dumosum Boiss., Iran, Sonboli et al. 1168 (MPH), AB683281, AB683395. T. elbursense Mozaff., Iran, Sonboli et al. 1109 (MPH), AB683282, AB683396. T. ferulaceum (Webb ex Berth.) Sch.-Bip., Spain, Canary Islands, Hultén s.n. (S), AB683283/AB683284, AB683397. T. germanicopolitanum (Bornm. et Heimerl) Grierson, Turkey, Bornmüller 14254 (S), AB683285, AB683398. T. griffithii (Clarke) Tzvel., Afghanistan, Rechinger 37485 (B), AB683286, AB683399. T. haradjanii (Rech. f.) Grierson, Turkey, Davis 16366 (M), AB683287, AB683400. T. haussknechtii (Bornm.) Grierson, Turkey, Dzudogru 1193 (HUB), AB683288, AB683401. T. hololeucum (Bornm.) Podl., Iran, Rechinger 6472 (S), AB683289, AB683402. T. joharchii Sonboli et Kaz. Osaloo, Sonboli et al. (2010), AB523746, AB683403. T. khorassanicum (Krasch.) Parsa, Iran, Rechinger 4937 (S), AB683290, AB683404. T. kotschyi (Boiss.) Grierson, Sonboli et al. (2010), AB523748, AB683405. T. kotschyi (Boiss.) Grierson, Gemeinholzer et al. (2006)/Iran, Rechinger 42053 (B), AJ880352/AB683292, AB683406. T. leptophyllum Stev., Caucasus, Daghestan, Becker s.n. (S), AB683293/AB683294, AB683407. T. microphyllum DC., Gemeinholzer et al. (2006)/Spain, Castroviejo 9855 (B), AJ880331/AB683296, AB683408. T. millefolium (L.) Tzvel., Bulgaria, Emanuelsson 3014 (S), AB683297/AB683298, AB683409. T. mucroniferum Huber-Mor. et Grierson, Turkey, Davis et Hedge 31785 (M), AB683299/AB683300, AB683410. T. nitens (Boiss. et Noe) Grierson, Turkey, Mucen 183 (W, V 1977-16564), AB683301, AB683411. T. paleaceum Podl., Afghanistan, Freitag 5828 (B), AB683302, AB683412. T. parthenifolium (Willd.) Sch.-Bip., Iran, Sonboli et al. 1127 (MPH), AB683303, AB683413. T. parthenium (L.) Sch.-Bip., Oberprieler (2004b), AJ864587/AJ864607, AB683414, T. parthenium (L.) Sch.-Bip., Sonboli and Oberprieler (2010), FN823080, AB683415. T. pinnatum Boiss., Iran, Sonboli et al. 1118 (MPH), AB683304, AB683416. T. pinnatum Boiss., Oberprieler (2004b), AJ864588/AJ864608, AB683417, T. polycephalum subsp. argyrophyllum (Koch.) Podl., Iran, Sonboli et al. 1125 (MPH), AB683305, AB683418. T. polycephalum subsp. duderanum (Boiss.) Podl., Iran, Rechinger 56842 (S), AB683306/AB683307, AB683419. T. polycephalum subsp. farsicum Podl., Iran, Sonboli et al. 1167 (MPH), AB683308, AB683420. T. porphyrostephanum (Rech. f.) Bremer et Humphries, Sonboli et al. (2010), AB523751, AB683421. T. poteriifolium (Ledeb.) Grierson, Syria, Wall 543c (S), AB683309/AB683310, AB683422. T. pseudachillea C. Winkl., Uzbekistan, Baranov et Schmidt 6734 (S), AB683311/AB683312, AB683423. T. punctatum (Desr.) Grierson, Oberprieler (2004b), AJ864589/AJ864609, AB683424. T. punctatum (Desr.) Grierson, Iran, Termeh et Moussavi 49833 (IRAN), AB683313, AB683425. T. roseum (Adams) Sch.-Bip., Georgia, Klackenberg 820629-2 (S), AB683314/AB683315, AB683426. T. salsugineum Podl., Iran, Mozaffarian s.n. (TARI), AB683316, AB683427. T. santolina Winkl., Kazakhstan, Androssov 3269a (S), AB683317/AB683318, AB683428. T. sclerophyllum H. Krasch., Russia, Gross 32700 (S), AB683319/AB683320, AB683429. T. siculum Strobl, Italy, Oberprieler 10349 (herb. Oberprieler), AB683321/AB683322, AB683430. T. sonbolii Mozaff., Iran, Sonboli et al. 998 (MPH), AB683323, AB683431. T. tabrisianum (Boiss.) Sosn. et Takht., Iran, Sonboli 1122 (MPH), AB683324, AB683432. T. tatsiense (Bur. et Franch.) Bremer et Humphries, China, Smith 10842 (S), AB683325/AB683326, AB683433. T. tenuisectum (Boiss.) Podl., Sonboli et al. (2010), AB523747, AB683434. T. turcomanicum (Kraschen.) Tzvel., Iran, Faghihnia et Zangooei 20867 (FUMH), AB683327, AB683435. T. uniflorum (Fisch. et C. A. Mey.) Sch.-Bip., Iran, Rechinger 41696 (S), AB683328/AB683329, AB683436. T. vahlii DC., Spain, Zubizarreta 12287 (B), AB683330/AB683331, AB683437. T. vulgare L., Germany, Oberprieler 9770 (herb. Oberprieler), AB683332/AB683333, AB683438. T. walteri (Winkl.) Tzvel., Iran, Rechinger 53283 (S), AB683334/AB683335, AB683439. T. zahlbruckneri (Nab.) Grierson, Iran, Alizadeh et al. 602 (MPH), AB683336, AB683440. Tripleurospermum caucasicum (Willd.) Hayek., Oberprieler (2004b), AJ864590/AJ864610, AB683441. T. perforatum (Merat) Laínz, Gemeinholzer et al. (2006)/Germany, Oberprieler 9764 (B), AJ880332/AB683338, AB683442. T. sevanense (Manden.) Pobed., Oberprieler (2004b), AJ864591/AJ864611, AB683443. T. transcaucasicum (Manden.) Pobed., Oberprieler (2004b), AJ864592/AJ864612, AB683444. Ursinia anthemoides (L.) Poir., Himmelreich et al. (2008), AM774473, AB683445. Xylanthemum fisherae (Aitch. et Hemsley) Tzvel., Sonboli and Oberprieler (2010), FN827333/FN827334, AB683446. X. paghmanense (Podl.) Bremer et Humphries, Afghanistan, (W-1986-05509), AB683339, AB683447. X. pamiricum (Hoffm.) Tzvel., Iran, Moussavi et Tehrani, 34987-E (IRAN), AB683340, AB683448. X. rupestre (M. Pop. ex Nevski) Tzvel., Afghanistan, Freitag 6388 (B), AB683341/AB683342, AB683449.

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Sonboli, A., Stroka, K., Kazempour Osaloo, S. et al. Molecular phylogeny and taxonomy of Tanacetum L. (Compositae, Anthemideae) inferred from nrDNA ITS and cpDNA trnH–psbA sequence variation. Plant Syst Evol 298, 431–444 (2012). https://doi.org/10.1007/s00606-011-0556-6

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Keywords

  • Asteraceae
  • Anthemideae
  • cpDNA
  • nrDNA
  • Phylogeny
  • Tanacetum
  • Taxonomy
  • Vogtia