Abstract
In this study, we tried to figure out phylogenetic relationships and taxonomical positions of closely related Muscari species. Four different cpDNA regions including both coding and non-coding ones, namely, matK, trnT(UGU)-trnL(UAA) intergenic spacer (IGS), trnL(UAA) intron and trnL(UAA)-F(GAA) IGS, were employed to determine the exact circumscription of three subgenera, Muscari, Leopoldia and Botryanthus. Seventy Muscari accessions representing 31 Muscari species and different number of previously published sequences retrieved from NCBI database were analyzed. The concatenated and matK data alone were observed to be informative while none of the used non-coding regions was suitable to determine phylogeny of Muscari. Concatenated alignment gave almost the same tree topology with matK sequence. Muscari azureum and M. coeleste phylogenetically separated from all other species of Botryanthus and four main clades were observed in both of the trees even though three subgenera are accepted by Flora of Turkey. After discussing the phylogenetic positions and morphological characters in detail, moving of these two species from Botryanthus to Pseudomuscari subgenus was suggested. Thus, this study proposes that the number of Muscari subgenera should be increased from three to four in Flora of Turkey. The position of M. mirum was also remarkable; it always located distantly to its relatives of Leopoldia. Although this species may also be distinguished based on morphological features such as quite shorter plant length, one or sometimes two relatively wider leaves, and a larger fruit, it needs further studies to resolve its position reliably. Interesting positions of other species were also discussed in detail based on morphological characters in the text.
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References
Anacker BL (2014) The nature of serpentine endemism. Am J Bot 101(2):219–224. https://doi.org/10.3732/ajb.1300349
Anacker BL, Whittall JB, Goldberg EE, Harrison SP (2011) Origins and consequences of serpentine endemism in the California flora. Evolution 65(2):365–376. https://doi.org/10.1111/j.1558-5646.2010.01114.x
Bogler D, Francisco-Ortega J (2004) Molecular systematic studies in cycads: evidence from trnL intron and ITS2 rDNA sequences. Bot Rev 70:260–273. https://doi.org/10.1663/0006-8101(2004)070[0260:MSSICE]2.0.CO;2
Böhnert T, Lobin W (2017) Leopoldia neumannii sp. nov. (Asparagaceae, Scilloideae): a new species of Muscari sensu lato from Greece. Willdenowia 47:179–185. https://doi.org/10.3372/wi.47.47210
Borzatti Von Loewenstern A, Giordani T, Astuti G, Andreucci A, Peruzzi L (2013) Phylogenetic relationships of Italian Bellevalia species (Asparagaceae), inferred from morphology, karyology and molecular systematics. Plant Biosyst 147:776–787. https://doi.org/10.1080/11263504.2013.829884
Buerki S, Jose S, Yadav SR, Goldblatt P, Manning JC, Forest F (2012) Contrasting biogeographic and diversification patterns in two Mediterranean-type ecosystems. PLoS One 7(6):e39377. https://doi.org/10.1371/journal.pone.0039377
Clegg MT, Zurawski G (1991) Chloroplast DNA and the study of plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 1–13
Cullen J, Knees SG, Cubey SH, Shaw JMH (2011) The European Garden Flora - flowering plants: a manual for the identification of plants cultivated in Europe both out-doors and under glass, 2nd Edn. Cambridge University Press, New York, pp 124–125
Czerepanov SK (1995) Vascular plants of Russia and adjacent states (the former USSR). Cambridge University Press, Cambridge, New York
Davis PH, Stuart DC (1980) Muscari Mill. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea 5. Cambridge University Press, Cambridge, pp 46–49
Davis PH, Stuart DC (1984) Muscari Mill. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands 8. Edinburgh University Press, Edinburgh, pp 245–263
Davis PH, Mill RR, Kit T (1988) Flora of Turkey and the East Aegean Islands, vol 10. Edinburgh University Press, Edinburgh
Demirci S, Özhatay N, Koçyiğit M (2013) Muscari erdalii (Asparagaceae, Scilloideae), a new species from southern Turkey. Phytotaxa 154:38–46. https://doi.org/10.11646/phytotaxa.154.1.2
Doyle JJ, Doyle JL (1987) A rapid DNA procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15 http://ci.nii.ac.jp/naid/10021087108/. Accessed 15 Aug 2018
Ekim T, Koyuncu M, Vural M, Duman H, Aytaç Z, Adıgüzel N (2000) Pteriophyta and Spermatophyta. Red Data Book of Turkish plants. Barışcan Ofset, Ankara
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Garbari F (2003) Muscari neglectum Guss. e M. atlanticum Boiss. et Reuter (Hyacinthaceae). Tipi, caratteristiche e considerazioni sulle due specie. Inform Bot Ital 35(2):329–336 http://www.societabotanicaitaliana.it/uploaded/60.pdf. Accessed 15 Aug 2018
Garbari F, Greuter W (1970) On the taxonomy and typification of Muscari Miller (Liliaceae) and allied genera, and on the typification of generic names. Taxon 19:329–334. https://doi.org/10.2307/1219056
Gielly L, Taberlet P (1994) The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. Mol Biol Evol 11:769–777. https://doi.org/10.1093/oxfordjournals.molbev.a040157
Govaerts R (2018) World checklist of Asparagaceae. Facilitated by the Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp/ Accessed 15 August 2018
Gürsoy M, Şık L (2010) Batı Anadolu’daki Muscari armeniacum Leichtlin ex Baker ve Muscari neglegtum Guss. türleri üzerinde karşılaştırmalı anatomik araştırmalar. Celal Bayar Üniversitesi Fen Bilimleri Dergisi 6(1):61–72 http://dergipark.gov.tr/cbayarfbe/issue/4049/53375. Accessed 15 Aug 2018
Heed Y (2010) Muscari armeniacum and M. polyanthum - one or two species. Dissertation, Department of Plant and Environmental Sciences University of Gothenburg
Herrmann H, Weiss G, Durka W (2005) Biological flora of Central Europe: Muscari tenuiflorum Tausch. Flora 201:81–101. https://doi.org/10.1016/j.flora.2005.03.002
Hilu KW, Liang H (1997) The matK gene: sequence variation and application in plant systematics. Am J Bot 84:830–839. https://doi.org/10.2307/2445819
Huelsenbeck JP, Ronquist F (2003) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Jafari A, Maassoumi AA (2011) Synopsis of Leopoldia, Muscari and Pseudomuscari (Hyacithaceae) in Iran, with Leopoldia ghouschtchiensis sp. nova. Ann Bot Fen 48:396–400. https://doi.org/10.5735/085.048.0502
Jafari A, Maassoumi AA, Farsi M (2008) Karyological study on Bellevalia and Muscari (Liliaceae) species of Iran. Asian J Plant Sci 7:50–59. https://doi.org/10.3923/ajps.2008.50.59
Johnson M, Özhatay N, Garbari F (1996) The genus Muscari (Hyacinthaceae) in Turkey: taxonomy, distribution and chromosome analysis. In: Öztürk MA et al (eds) Plant life In Southwest and Central Asia. Ege Univ. Press, İzmir, pp 34–53
Karlén T (1991) Muscari Miller. In: Strid A, Tan K (eds) Mountain Flora of Greece, vol 2. Edinburgh Univ. Press, Edinburgh, pp 697–701
Kaya E (2014) Muscari Mill. In: Türkiye Geofitleri, vol. 2. Atatürk Bahçe Kültürleri Merkez Araştırma Enstitüsü, Yayın No: 96, Yalova, Turkiye, pp 350–411
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li JH, Bogle AL, Klein AS (1997) Interspecific relationships and genetic divergence of the disjunct genus Liquidambar (Hamamelidaceae). Rhodora 99:229–241 https://www.jstor.org/stable/23313320. Accessed 15 Aug 2018
Martínez-Azorín M, Crespo MB, Juan A, Fay MF (2011) Molecular phylogenetics of subfamily Ornithogaloideae (Hyacinthaceae) based on nuclear and plastid DNA regions, including a new taxonomic arrangement. Ann Bot 107:1–37. https://doi.org/10.1093/aob/mcq207
Nersesian A (2001) A karyosystematic study of Armenian Muscari and Bellevalia (Hyacinthaceae). Bocconea 13:383–389 http://147.163.105.223/bocconea/13-383.pdf. Accessed 15 Aug 2018
Özhatay N (2000) Muscari Miller. In: Güner A, Özhatay N, Ekim T, Başer KHC (eds) Flora of Turkey and the East Aegean Islands, vol 11. Edinburgh University Press, Edinburgh, pp 237–240
Özhatay N, Kültür Ş (2006) Check-list of additional taxa to the supplement Flora of Turkey III. Turk J Bot 30:281–316 http://journals.tubitak.gov.tr/botany/abstract.htm?id=8420. Accessed 15 Aug 2018
Özhatay N, Kültür Ş, Aslan S (2009) Check-list of additional taxa to the supplement Flora of Turkey IV. Turk J Bot 33:191–226. https://doi.org/10.3906/bot-0805-12
Özhatay FN, Kültür Ş, Gürdal MB (2011) Check-List of additional taxa to the supplement Flora of Turkey V. Turk J Bot 35:589–624. https://doi.org/10.3906/bot-1101-20
Pfosser M, Speta F (1999) Phylogenetics of Hyacinthaceae based on plastid DNA sequences. Ann Mo Bot Gard 86:852–875. https://doi.org/10.2307/2666172
Pınar SM, Fidan M, Eroğlu H (2018) Muscari botryoides (L.) Mill.: a new record for the family Asparagaceae from Turkey. Turk. J Agric Res 5(2):116–119. https://doi.org/10.19159/tutad.368374
Pirhan AF, Yıldırım H, Altıoğlu Y (2014) Muscari serpentinicum sp. nova (Asparagaceae): a new species from western Anatolia, Turkey. Ot Sistematik Botanik Dergisi 21(1):1–14
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Ruiz Rejón M, Oliver JL (1981) Genetic variability in Muscari comosum (Liliaceae). I. A comparative analysis of chromosome polymorphisms in Spanish and Aegean populations. Heredity 47(3):403–407. https://doi.org/10.1038/hdy.1981.101
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92(1):142–166. https://doi.org/10.3732/ajb.92.1.142
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94(3):275–288. https://doi.org/10.3732/ajb.94.3.275
Small RL, Lickey EB, Shaw J, Hauk WD (2005) Amplification of noncoding chloroplast DNA for phylogenetic studies in lycophytes and monilophytes with a comparative example of relative phylogenetic utility from Ophioglossaceae. Mol Phylogenet Evol 36(3):509–522. https://doi.org/10.1016/j.ympev.2005.04.018
Speta F (1989) Muscari (subg. Leopoldia) mirum Speta, spec. nova, im Kreise seiner nächsten Verwandten. Phyton (Austria) 29(1):105–117
Speta F (1998) Hyacinthaceae. In: Kubitzki K (ed) The families and genera of vascular plants III. Springer, Berlin, pp 261–285
Suárez-Santiago VN, Salinas JS, Romero-García AT, Garrido-Ramos MA, de la Herran R, Ruiz-Rejón C, Ruiz-Rejón M, Blanca G (2007) Polyploidy, the major speciation mechanism in Muscari subgenus Botryanthus in the Iberian Peninsula. Taxon 56:1171–1184. https://doi.org/10.2307/25065910
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. https://doi.org/10.1007/bf00037152
Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E (2007) Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Res 35(3):e14. https://doi.org/10.1093/nar/gkl938
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752
Turktas M, Aslay M, Kaya EF (2012) Molecular characterization of phylogenetic relationships in Fritillaria species inferred from chloroplast trnL-trnF sequences. Turk J Biol 36:552–560. https://doi.org/10.3906/biy-1201-30
Uysal T, Ertuğrul K, Dural H, Küçüködük M (2007) Muscari turcicum (Liliaceae/Hyacinthaceae), a new species from South Anatolia. Bot J Linn Soc 154:233–236. https://doi.org/10.1111/j.1095-8339.2007.00646.x
Valdés B, Lifante ZD (1992) Karyology and reproductive biology of Muscari matritensis M. Ruíz Rejón et al. (Liliaceae). Bot J Linn Soc 109:125–130. https://doi.org/10.1111/j.1095-8339.1992.tb00261.x
Yang J, Vázquez L, Chen X, Li H, Zhang H, Liu Z, Zhao G (2017) Development of chloroplast and nuclear DNA markers for Chinese Oaks (Quercus Subgenus Quercus) and assessment of their utility as DNA barcodes. Front Plant Sci 8:816. https://doi.org/10.3389/fpls.2017.00816
Yıldırım H (2015) Muscari atillae (Asparagaceae): a new species from eastern Anatolia, Turkey. Phytotaxa 213(3):291–295. https://doi.org/10.11646/phytotaxa.213.3.9
Yıldırım H (2016) Muscari elmasii sp. nova (Asparagaceae): a new species from western Anatolia, Turkey. Turk J Bot 40:380–387. https://doi.org/10.3906/bot-1507-17
Yıldırımlı Ş (2011) Three new species from Turkey. Ot Sistematik Botanik Dergisi 18(1):1–12
Yilmaz H, Yilmaz OY, Akyüz YF (2017) Determining the factors affecting the distribution of Muscari latifolium, an endemic plant of Turkey, and a mapping species distribution model. Ecol Evol 7(4):1112–1124. https://doi.org/10.1002/ece3.2766
Acknowledgements
This research was supported by The Scientific and Technological Research Council of Turkey (TUBİTAK; grant no. 114Z736). We sincerely thank “anonymous” reviewers and the managing editor, Katarina Hegedusova, for their constructive criticisms that improved the manuscript.
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Appendix 1. Species of which sequences were retrieved from NCBI
Appendix 1. Species of which sequences were retrieved from NCBI
Region matK: M. aucheri (HM640628), M. armeniacum (MF349951), M. neglectum (JX090381).
Region trnL intron: Muscari botryoides (AJ232545), M. macrocarpum (AJ232544), M. comosum (AJ232546, FJ423215), M. parviflorum (AJ508003).
Region trnL-F IGS: Muscari comosum (FJ423215, AJ232669), M. botryoides (AJ232668), M. macrocarpum (AJ232667)
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Dizkirici, A., Yigit, O., Pinar, M. et al. Molecular phylogeny of Muscari (Asparagaceae) inferred from cpDNA sequences. Biologia 74, 205–214 (2019). https://doi.org/10.2478/s11756-018-00164-0
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DOI: https://doi.org/10.2478/s11756-018-00164-0