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Phylogeny, biogeography, and character evolution in the genus Scilla s.l. and its close relatives Chionodoxa, Gemicia, Puschkinia, and Prospero (Asparagaceae)

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Abstract

Scilla s.l. is taxonomically one of the most problematic genera of the Asparagaceae. Within the last few decades, several genera were segregated from this genus; however, there is still no consensus on the taxonomic status of Scilla segregates. Although some previous studies indicated a polyphyletic origin for the genus Scilla, there has been no comprehensive phylogenetic study focusing on the entire complex including Chionodoxa, Prospero, Puschkinia, and the recently described Gemicia. To achieve this, we evaluated three plastid regions, namely rbcL, trnL-F, and matK, for 79 accessions. The monophyly of Puschkinia and Prospero was supported by our phylogenetic analyses; however, Chionodoxa and Gemicia were placed into a clade with representatives of the S. bifolia species group. While our divergence time estimation analysis indicated a Miocene origin for all studied genera of polyphyletic Scilla s.l., the results of our ancestral area and ancestral state analyses showed that Scilla, Prospero, Chionodoxa, and Puschkinia, together with Brimeura Salisb., Bellevalia, Hyacinthella, and Alrawia, probably had a most recent common ancestor without a perianth tube and a corona, and with a non-papillate testa surface, which evolved about 36 Ma in the Mediterranean region.

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Data availability

The GenBank accession numbers for all successfully sequenced trnL-F, rbcL, and matK DNA barcodes can be found in “Appendix”.

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Acknowledgments

The authors would like to thank Mehmet Fırat (Van, Turkey) for providing certain plant material used in this work and Leslie Demir for her support in language edition.

Funding

This work was financially supported by the Ege University Scientific Research Projects Coordination Unit (Project Number: 2011 BBH 002) and TÜBİTAK (Project Numbers: 106T598 and 116Z573).

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Hacettepe University, 06800, Beytepe, Ankara, Turkey

    Barış Özüdoğru & Burcu Tarıkahya Hacıoğlu

  2. Biological Diversity Research and Application Centre, Hacettepe University, 06800, Beytepe, Ankara, Turkey

    Barış Özüdoğru

  3. Department of Plant and Animal Production, Çiçekdağı Vocational College, Kırşehir Ahi Evran University, Çiçekdağı, Kırşehir, Turkey

    Deniz Aygören Uluer

  4. Department of Biology, Faculty of Science, Ege University, 35100, Bornova, İzmir, Turkey

    Hasan Yıldırım

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  1. Barış Özüdoğru
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  2. Deniz Aygören Uluer
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Contributions

BÖ and HY designed the study; HY provided the plant materials; BÖ and HY funded the research; BÖ and BTH performed the molecular work; DAU analyzed data with input from BÖ; BÖ and HY prepared figures; BÖ and DAU wrote the manuscript with contributions from HY and BTH.

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Correspondence to Barış Özüdoğru.

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Appendices

Appendix

Taxon sampling of the current study based on matK, trnL-F, and rbcL plastid regions. Information is presented in the following order: taxon name and voucher number; locality; GenBank accession numbers for matK, trnL-F, and rbcL. A dash (-) indicates that the region could not be sampled.


Hyacinthaceae. Scilla L.: × Chionoscilla allenii HY2296; İzmir, Nif Mountain; OM972799, OM994077, OM972798. Chionodoxa forbesii Baker HY2294; Muğla, Fethiye, Babadağ; OM972800, OM994028, OM972737. C. luciliae Boiss. HY2344 İzmir, Ödemiş, Bozdağ; OM972801, OM994029, OM972738. C. salbacus Yıldırım HY2797; Denizli, Babadağ, at the bottom of Karababa Hill; OM972850, OM994030, OM972739. C. sardensis Whittall ex Barr & Sugden HY2298; İzmir, Mahmut Mountain; OM972802, OM994031, OM972740. C. siehei Stapf. HY2295; İzmir, Nif Mountain; OM972803, OM994032, OM972741. Scilla albinerve Yıldırım & Gemici HY2251; Hatay, Arsuz, Amanos Mountains; OM972806, OM994044, OM972758. S. alinihatiana Aslan &Yıldırım HY2944; Rize, İkizdere, from Sivrikayalar to highland; OM972804, OM994042, OM972756. S. alinihatiana HY2936; Artvin, Yusufeli, Marsis Mountain; OM972805, OM994043, OM972757. S. bifolia L. BO3758; Çankırı, Ilgaz, Şeyhyunus village; OM972807, OM994047, OM972765. S. bifolia BO3804a; Isparta, Dedegöl Mountain; OM972808, OM994046, OM972764. S. bifolia BO3814; Muğla, Fethiye, Tuzlabeli; OM972809, -, OM972763. S. bifolia HY2293; Muğla, Köyceğiz, Sandras Mountain; OM972811, -, OM972761. S. bifolia HY2246; İzmir, Bozdağ; -, -, OM972759. S. bifolia HY3771; Belgrad Forest; OM972813, OM994049, OM972767. S. bifolia HY1495; Nif Mountain; OM972814, OM994048, OM972766. S. bilgineri Yıldırım HY2788; Adıyaman, Gölbaşı; -, OM994050, OM972768. S. bithynica Boiss. HY3774; Adapazarı, Gevye, Doğançay village; OM972815, OM994052, OM972770. S. bithynica HY2787; Bartın, Karagoguz Hill, Arıtolu; OM972816, OM994051, OM972769. S. cilicica Siehe HY2289; Mersin, Erdemli, Lomes Canyon; OM972817, OM994053, OM972771. S. hakkariensis Fırat & Yıldırım MF28629; Derecik; OM972818, OM994069, OM972790. S. hyacinthoides L. HY3770; Muğla, Datça, Yakaköy; OM972819, -, OM972773. S. hyacinthoides AG13597; Gaziantep, İslahiye, Yesemek Open Air Museum; OM972820, -, OM972772. S. ingridae Speta HY2288; Adana, Pozantı, Akçatekir Highland; OM972821, OM994058, OM972779. S. ingridae HY1346; Adana, Tufanbeyli; -, -, OM972774. S. ingridae HY2286; Kahramanmaraş, Andırın; OM972822, OM994057, OM972778. S. ingridae HY2254; Adana, Aladağlar, Maden Pass; OM972823, OM994054, OM972775. S. ingridae BO4968; Kayseri, Dededağı; OM972824, OM994059, OM972780. S. ingridae HY2256_1; Gaziantep, Nurdağı Pass; OM972825, OM994055, OM972776. S. ingridae HY2256_2; Gaziantep, Nurdağı Pass; -, OM994056, OM972777. S. leepii Speta HY2266; Malatya, Doğanşehir; OM972826, OM994060, OM972781. S. leepii MF30501; Çatak; OM972827, OM994065, OM972786. S. leepii HY2285; Van, Çatak Canyon; OM972828, OM994064, OM972785. S. leepii HY2278; Elazığ, on the Maden-Ergani road; OM972829, OM994062, OM972783. S. leepii HY2281; Siirt, Şirvan, on the Nallıkaya road; OM972830, OM994063, OM972784. S. leepii HY2273; Adıyaman, Nemrut Mountain; OM972831, OM994061, OM972782. S. madeirensis Menezes Chase 37,839; Madeira; JX090401, -, JX090589. S. melaina Speta HY2250; Hatay, Dörtyol, Kuzuculu; OM972832, OM994067, OM972788. S. melaina HY2253; Hatay, Atik Plateau; OM972833, OM994066, OM972787. S. mesopotamica Speta HY2261; Şanlıurfa, Halfeti; OM972834, OM994068, OM972789. S. messeniaca Boiss. Chase 1718; Greece; JX090402, JX090480, JX090590. S. monanthos K.Koch HY2347; Rize, Çamlıhemşin, Ayder Highland; -, OM994070, OM972791. S. persica Hausskn. MF30545; Siirt, Şirvan district, Herzane Hill; OM972835, OM994071, OM972792. S. persica MF30590; Şırnak, Besta Dereler; OM972836, OM994072, OM972793. S. peruviana L. Chase 1619; Tunisia; AJ581423, JX090481, JX090591. S. rosenii K.Koch HY2349; Ardahan, Yalnızçam Mountains; OM972837, OM994073, OM972794. S. siberica subsp. armena (Grossh.) Mordak HY2352; Kars, Sarıkamış, Çamyazı village; OM972838, OM994075, OM972796. S. siberica subsp. armena HY1442; Erzurum, Şenkaya; -, OM994074, OM972795. S. siberica subsp. caucasica (Miscz.) Mordak HY2346; Trabzon, Şalpazarı, Sisdağı; OM972839, OM994076, OM972797. S. taurica Fuss. HY2345; Trabzon, Şalpazarı, Sisdağı; OM972810, OM994045, OM972762. S. taurica HY2283; Siirt, Şirvan, Gökbudak, Belenoluk; OM972812, -, OM972760. S. verna Huds. Chase 8288; England; JX090403, JX090482, JX090592. Puschkinia Adams., P. bilgineri Yıldırım HY2918; Van, Karabet Pass; OM972840, OM994039, OM972749. P. peshmenii Rix & B.Mathew HY1151; Hakkari, Yüksekova; -, -, OM972750. P. scilloides Adams HY2271; Malatya, Pötürge, on the Nemrut Mountain road; OM972841, OM994040, OM972754. P. scilloides HY2354; Van, Gevaş, Artos Mountain; OM972842, OM994041, OM972755. P. scilloides HY1125; Van, Deveboynu Peninsula; -, -, OM972751. P. scilloides HY1156; Van, Güzelsu, Güzeldere; -, -, OM972752. P. scilloides HY1410; Van, Oruçlu; -, -, OM972753. P. scilloides Chase 21,560; Lebanon; JX090397, JX090476, JX090585. Gemicia Yıldırım.: G. vardariana Yıldırım & Gemici HY2348; Rize, Çamlıhemşin, Ayder Highland; OM972843, OM994033, OM972742. Prospero Salisb.: P. autumnale (L.) Speta HY3758; Muğla, Marmaris, Taşlıca village; OM972844, OM994038, OM972747. P. autumnale HY1478; Denizli, Servergazi; OM972845, OM994036, OM972745. P. autumnale HY2292; Muğla, Köyceğiz, Sandras Mountain, Beyobası; OM972846, OM994037, OM972746. P. cudidaghense Fırat & Yıldırım M.Fırat 30575; Şırnak, Silopi, Cudi Mountain; OM972847, -, OM972748. Hyacinthella Schur.: H. acutiloba K.Perss. & Wendelbo HY1366; Malatya, Darende, Akçababalı Mountain; OM972848, OM994034, OM972743. H. glabrescent (Boiss.) K.Perss. & Wendelbo HY2288a; Adana, Pozantı, Akçatekir Highland; OM972849, OM994035, OM972744. Bellevalia Lapeyr.: B. fominii Woronow Chase 1727; Turkey; JX090318, JX090493, JX090415. B. longistyla (Miscz.) Grossh. Chase 1611; Turkey; JX090320, JX090495, JX090417. B. pseudolongipes Karabacak & Yıldırım OK8275; Siirt, Siirt University, Kezer Campus; -, -, OM972736. Fessia Speta.: F. vvedenskyi (Pazij) Speta Chase 1688; Tajikistan; JX090361, JX090540, JX090444. F. hohenackeri (Fisch. & C.A.Mey.) Speta Mario Martínez & Julio Pati_o S09; Spain; JX090360, JX090539, JX090443. Alrawia (Wendelbo) Perss. & Wendelbo.: A. bellii (Baker) Perss. & WendelboChase 1510; Iran; JX090315, AM902384/AM902479, AM902332. Muscari Mill.: M. neglectum Guss. ex Ten. Chase 21,836; Turkey; JX090381, JX090562, Z77278. Brimeura Salisb.: B. amethystina (L.) Chouard. Chase 1777; Spain; JX090326, JX090501, JX090422. OUTGROUPS. Lachenalia pusilla Jacq. Manning s.n.; South Africa; JX090375, JX090452, JX090554. Ledebouria nossibeensis (H.Perrier) J.C.Manning & Goldblatt MP53990; Madagascar; JX090376, JX090453, AM909711. (Baker) J.C.Manning & Goldblatt 11,258; South Africa; JX090348, JX090434, JX090522. Ornithogalum orthophyllum Ten. Chase 1823; Greece; JX090391, JX090467, JX090574.

Information on Electronic Supplementary Material

Online Resource 1. Input matrix for the ancestral area and state reconstructions.

Online Resource 2. Lagrange results of ancestral area reconstruction.

Online Resource 3. Results of character reconstruction for presence or absence of perigone tubeancestral.

Online Resource 4. Results of character reconstruction for presence or absence of corona.

Online Resource 5. Ancestral state reconstruction of the “presence or absence of corona”.

Online Resource 6. Results of character reconstruction for testa surface papillate or not.

Online Resource 7. Ancestral state reconstruction of the “testa surface”.

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Özüdoğru, B., Aygören Uluer, D., Tarıkahya Hacıoğlu, B. et al. Phylogeny, biogeography, and character evolution in the genus Scilla s.l. and its close relatives Chionodoxa, Gemicia, Puschkinia, and Prospero (Asparagaceae). Plant Syst Evol 308, 44 (2022). https://doi.org/10.1007/s00606-022-01835-x

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