Sevcan ÇELENK, Gülnar İSMAILOVA, Bayram YILDIZ, Tuncay DİRMENCİ, Taner ÖZCAN, Turan ARABACI

Hybridization among three Cirsium (Asteraceae) species and important evidence for three new hybrids from Turkey

In this study, three new hybrids from the genus Cirsium are described for the first time. Cirsium ×nezaketiae Yıldız, Dirmenci& Arabacı, C. ×kelkitensis Yıldız, Arabacı & Dirmenci, and C. ×erzincanicum Yıldız, Dirmenci & Arabacı are investigated in detailmorphologically, palynologically, and molecularly. The hybrid individuals were detected on field trips due to their intermediatemorphological characters. Their morphological properties were analyzed to compare with their parents. The pollen grain morphologiesof the hybrids and their allies were investigated using light and a scanning electron microscope. The pollen grains were radiallysymmetrical, isopolar, trizonocolporate, and with echinate or scabrate sculpturing. The tectum is psilate/punctate, microreticulate,or ornate in sculpture. Dimorphic pollen grains were encountered in C. leucocephalum (Willd.) Spreng. subsp. leucocephalum. Twonuclear DNA regions were used to find single nucleotide polymorphisms. nrITS DNA data gave more information than nrETS dataabout polymorphism. In conclusion, C. ×nezaketiae, C. ×kelkitensis, and C. ×erzincanicum exhibit some significant morphological,palynological, and molecular differences from their parents and present evidence of potential introgression hybridization. Since thehybrids live in a complex with their parents, and some parents have polymorphic loci like their putative hybrids, it can be presented asevidence for potential introgression since backcrossing may be possible among taxa.

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Baker HG (1955). Pollen dimorphism in the Rubiacae. Evolution 10: 23-31.
Baldwin BG, Markos S (1998). Phylogenetic utility of the external transcribed spacer (ETS) of 18S-26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Mol Phylogenet Evol 10: 449-463.
Bloom W (1977). Chromosomal differentiation between Cirsium discolor and C. muticum and the origin of supernumerary chromosomes. Syst Botany 2: 1-13.
Bureš P, Smarda P, Rotreklová O, Oberreiter M, Buresova M, Konecny J, Knoll A, Fajmon K, Smerda J (2010). Pollen viability and natural hybridization of Central European species of Cirsium. Preslia 82: 391-422.
Bureš P, Smerda J, Michalkova E, Smarda P, Knoll A, Vavrinec M (2018). Cirsium greimleri: a new species of thistle endemic to the Eastern Alps and Dinarides. Preslia 90: 105-134.
Bureš P, Wang YF, Horova L, Suda J (2004) Genome size variation in Central European species of Cirsium (Compositae) and their natural hybrids. Ann Bot London 94: 353-363.
Chan R, Baldwin BG, Ornduff R (2001). Goldfields revisited: a molecular phylogenetic perspective on the evolution of Lasthenia (Compositae: Heliantheae sensu lato). Int J Plant Sci 162: 1347-1360.
Charadze AL (1963). Cirsium Mill. In: Bobrov EG, Cherepanov SK (editors). Flora of the USSR, Vol. XXVIII. Moscow, USSR: Izdatel’stvo Akademii Nauk SSSR, pp. 63-270.
Clevinger JA, Panero JL (2000). Phylogenetic analysis of Silphium and subtribe Engelmanniinae (Asteraceae: Heliantheae) based on ITS and ETS sequence data. Am J Botany 87: 565-572.
Currat M, Ruedi M, Petit RJ, Excoffier L (2008). The hidden side of invasions: massive introgression by local genes. Evolution 62: 1908-1920.
Czapik R (1958). Karyological studies in species of Cirsium Mill. em. Scop. occurring in Poland. Acta Soc Bot Pol 27: 483-489. Dabydeen S (1987). Natural hybridization in the genus Cirsium: C. flodmanii × C. undulatum. Rhodora 89: 369-373.
Davidson R (1963). Initial biometric survey of morphological variation in Cirsium altrissimum-C. discolor complex. Brittonia 15: 222-241.
Davis PH, Parris SB (1975). Cirsium Mill. In: Davis PH (editor). Flora of Turkey and the East Aegean Islands, Vol. 5. Edinburgh, UK: Edinburgh University Press, pp. 370-412.
Davis PH, Tan K, Mill RR (editors) (1988). Flora of Turkey and the East Aegean Islands, Vol. 10 (Suppl. 1). Edinburgh, UK: Edinburgh University Press.
Dirmenci T, Özcan T, Yazıcı T, Arabacı T, Martin E (2018a). Morphological, cytological, palynological and molecular evidence on two new hybrids: an example of homoploid hybridization in Origanum (Lamiaceae). Phytotaxa 371: 145- 167.
Dirmenci T, Yazıcı T, Özcan T, Çelenk S, Martin E (2018b). A new species and a new natural hybrid of Origanum L. (Lamiaceae) from the west of Turkey. Turk J Bot 42: 73-90.
Erdtman G (1952). Pollen Morphology and Plant Taxonomy— Angiosperms. Stockholm, Sweden: Almqvist and Wiksell. Erşen Bak F, Özcan M (2018). Pollen morphology of endemic NE Anatolian Cirsium taxa (Asteraceae). Pak J Bot 50: 1181-1185.
Faegri K, Iversen J (1989). Textbook of Pollen Analysis. 4th ed. Chichester, UK: Wiley.
Garcia-Jacas N, Garnatje T, Susanna A, Vilatersana R (2002). Tribal and subtribal delimitation and phylogeny of the Cardueae (Asteraceae): a combined nuclear and chloroplast DNA analysis. Mol Phylogenet Evol 22: 51-64.
Güner A, Özhatay N, Ekim T, Başer KHC (editors) (2000). Flora of Turkey and the East Aegean Islands, Vol. 11 (Suppl. 2). Edinburgh, UK: Edinburgh University Press.
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4: 1-9.
Hesse M, Halbritter H, Zetter R, Weber M, Buchner R, FroschRadivo A, Ulrich S (2009). Pollen Terminology. An Illustrated Handbook. New York, NY, USA: Springer.
Jacquemyn H, Brys R, Honnay O, Roldán-Ruiz I, Lievens B, Wiegand T (2012). Nonrandom spatial structuring of orchids in a hybrid zone of three Orchis species. New Phytol 193: 454-464.
Jaźwa M, Jedrzejczak E, Klichowska E, Pliszko A (2018). Predicting the potential distribution area of Solidago ×niederederi (Asteraceae). Turk J Bot 42: 51-56.
Jolliffe IT (2002). Principal Component Analysis. New York, NY, USA: Springer Verlag.
Jump AS, Dawson DA, James CM, Woodward FI, Burke T (2002). Isolation of polymorphic microsatellites in the stemless thistle (Cirsium acaule) and their utility in other Cirsium species. Mol Ecol Notes 2: 589-592. References DİRMENCİ et al. / Turk J Bot 384
Kadereit JW, Jeffrey C (editors) (2007). Flowering Plants. Eudicots: Asterales. Berlin, Germany: Springer.
Kaplan Z, Fehrer J (2007). Molecular evidence for a natural primary triple hybrid in plants revealed from direct sequencing. Ann Bot 99: 1213-1222.
Keil DJ (2006). Cirsium Mill. In: Flora of North America Editorial Committee (editors). Flora of North America North of Mexico, Vol. 19. New York, NY, USA: Oxford University Press, pp. 95- 164.
Kelch DG, Baldwin BG (2003). Phylogeny and ecological radiation of New World thistles (Cirsium, Cardueae Compositae) based on ITS and ETS rDNA sequence data. Mol Ecol 12: 141-151.
Kim SC, Graham SA, Graham A (1994). Palynology and pollen dimorphism in the genus Lagerstroemia (Lythraceae). Grana 33: 1-20.
Kita Y, Ueda K, Kadota Y (1995). Molecular phylogeny and evolution of the Asian Aconitum subgenus Aconitum (Ranunculaceae). J Plant Res 108: 429-442.
Kokubugata G, Kurihara T, Hirayama Y, Obata K (2011). Molecular evidence for a natural hybrid origin of Ajuga ×mixta (Lamiaceae) using ITS sequence. Bulletin of the National Museum of Natural Science 37: 175-179.
Lee J, Baldwin BG, Gottlieb LD (2002). Phylogeny of Stephanomeria and related genera (Compositae–Lactuceae) based on analysis of 18S-26S nuclear rDNA ITS and ETS sequences. Am J Botany 89: 160-168.
Linder CR, Goertzen LR, Heuvel BV, Francisco-Ortega J, Jansen RK (2000). The complete external transcribed spacer of 18S-26S rDNA: amplification and phylogenetic utility at low taxonomic levels in Asteraceae and closely allied families. Mol Phylogenet Evol 14: 285-303.
Mallet J (2005). Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229-237.
Markos S, Baldwin BG (2001). Higher-level relationships and major lineages of Lessingia (Compositae, Astereae) based on nuclear rDNA internal and external transcribed spacer (ITS and ETS) sequences. Syst Botany 26: 168-183.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2011). B-Chromosome and cytomixis in Cirsium (Asteraceae). Cytologia 76: 41-47.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2012). Pollen morphological studies on the genus Cirsium Mill. (Asteraceae) in Iran. J Japanese Bot 87: 268-279.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2013). ISSR and RAPD analyses of species and their relationships in the genus Cirsium (Asteraceae) in Iran. Phytologia Balcanica 19: 225-232.
Ownbey G (1951). Natural hybridization in the genus Cirsium-I. C. discolor (Mubl. ex Willd.) Spreng. × C. muticum Mich. Bulletin of the Torrey Botanical Club 37: 541-547.
Ownbey G (1964). Natural hybridization in the genus Cirsium-II. C. altissimum × C. discolor. Michigan Bot 1: 87-97. Ozcan M, Hayirlioglu-A
Kadereit JW, Jeffrey C (editors) (2007). Flowering Plants. Eudicots: Asterales. Berlin, Germany: Springer.
Kaplan Z, Fehrer J (2007). Molecular evidence for a natural primary triple hybrid in plants revealed from direct sequencing. Ann Bot 99: 1213-1222.
Keil DJ (2006). Cirsium Mill. In: Flora of North America Editorial Committee (editors). Flora of North America North of Mexico, Vol. 19. New York, NY, USA: Oxford University Press, pp. 95- 164.
Kelch DG, Baldwin BG (2003). Phylogeny and ecological radiation of New World thistles (Cirsium, Cardueae Compositae) based on ITS and ETS rDNA sequence data. Mol Ecol 12: 141-151.
Kim SC, Graham SA, Graham A (1994). Palynology and pollen dimorphism in the genus Lagerstroemia (Lythraceae). Grana 33: 1-20.
Kita Y, Ueda K, Kadota Y (1995). Molecular phylogeny and evolution of the Asian Aconitum subgenus Aconitum (Ranunculaceae). J Plant Res 108: 429-442.
Kokubugata G, Kurihara T, Hirayama Y, Obata K (2011). Molecular evidence for a natural hybrid origin of Ajuga ×mixta (Lamiaceae) using ITS sequence. Bulletin of the National Museum of Natural Science 37: 175-179.
Lee J, Baldwin BG, Gottlieb LD (2002). Phylogeny of Stephanomeria and related genera (Compositae–Lactuceae) based on analysis of 18S-26S nuclear rDNA ITS and ETS sequences. Am J Botany 89: 160-168.
Linder CR, Goertzen LR, Heuvel BV, Francisco-Ortega J, Jansen RK (2000). The complete external transcribed spacer of 18S-26S rDNA: amplification and phylogenetic utility at low taxonomic levels in Asteraceae and closely allied families. Mol Phylogenet Evol 14: 285-303.
Mallet J (2005). Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229-237.
Markos S, Baldwin BG (2001). Higher-level relationships and major lineages of Lessingia (Compositae, Astereae) based on nuclear rDNA internal and external transcribed spacer (ITS and ETS) sequences. Syst Botany 26: 168-183.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2011). B-Chromosome and cytomixis in Cirsium (Asteraceae). Cytologia 76: 41-47.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2012). Pollen morphological studies on the genus Cirsium Mill. (Asteraceae) in Iran. J Japanese Bot 87: 268-279.
Nouroozi M, Sheidai M, Attar F, Noormohammadi Z (2013). ISSR and RAPD analyses of species and their relationships in the genus Cirsium (Asteraceae) in Iran. Phytologia Balcanica 19: 225-232.
Ownbey G (1951). Natural hybridization in the genus Cirsium-I. C. discolor (Mubl. ex Willd.) Spreng. × C. muticum Mich. Bulletin of the Torrey Botanical Club 37: 541-547.
Ownbey G (1964). Natural hybridization in the genus Cirsium-II. C. altissimum × C. discolor. Michigan Bot 1: 87-97.
Ozcan M, Hayirlioglu-Ayaz S, Inceer H (2008). Chromosome counts of some Cirsium (Asteraceae, Cardueae) taxa from Turkey. Caryologia 6: 375-382.
Ozcan M, Hayirlioglu-Ayaz S, Inceer H (2011). Chromosome reports in some Cirsium (Asteraceae, Cardueae) taxa from north-east Anatolia. Caryologia 64: 55-66.
Petrak F (1979). Cirsium Mill. In: Rechinger KH (editor). Flora Iranica. Compositae III-Cynareae, Vol. 139a. Graz, Austria: Akademische Druck-u Verlagsanstalt, pp. 231-280.
Polat N, Kıran Y, Şahin A, Yıldız B, Arabacı T (2018). Chromosome counts and karyotype analysis of some representatives of genus Cirsium Mill. (Asteraceae) in Turkey. Caryologia 71: 133-138.
Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007). Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143: 1-81.
Romesburg HC (2004). Cluster Analysis for Researchers. Raleigh, NC, USA: Lulu Press.
Rotreklová O, Bureš P, Grulich V (2004). Chromosome numbers for some species of vascular plants from Europe. Biologia 59: 425- 433.
Segarra-Moragues JG, Villar L, Lopez J, Perez-Collazos E, Catalan P (2007). A new Pyrenean hybrid Cirsium (Asteraceae) as revealed by morphological and molecular analyses. Bot J Linn Soc 154: 421-434.
Seif E, Sheidai M, Nouroozi M, Noormohammadi Z (2012). Biosystematic studies of Cirsium arvense populations in Iran. Phytologia Balcanica 18: 279-288.
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: 275-288.
Sheidai M, Seif M, Nouroozi M, Noormohammadi Z (2012). Cytogenetic and molecular diversity of Cirsium arvense (Asteraceae) populations in Iran. J Japanese Bot 87: 193-205.
Slotta TAB, Horvath DP, Foley ME (2012). Phylogeny of Cirsium spp. in North America: host specificity does not follow phylogeny. Plants 1: 61-73.
Stanford AM, Harden R, Parks CR (2000). Phylogeny and biogeography of Juglans (Juglandaceae) based on matK and ITS sequence data. Am J Bot 87: 872-882.
Susanna A, Garcia-Jacas N, Soltis DEPS, Soltis PS (1995). Phylogenetic relationships in tribe Cardueae (Asteraceae) based on ITS sequences. Am J Bot 82: 1056-1068.
Swofford DL (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, MA, USA: Sinauer Associates.
Valtuena FJ, Preston CD, Kadereit JW (2011). Evolutionary significance of the invasion of introduced populations into the native range of Meconopsis cambrica. Mol Ecol 20: 4318-4331.
Werner K (1976). Cirsium Mill. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Web DA (editors). Flora Europaea, Vol. 4. Cambridge, UK: Cambridge University Press, pp. 232-242.
White TJ, Bruns T, Lee S, Taylor J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand DH, Sninsky JJ, White TJ (editors). PCR Protocols: A Guide to Methods and Applications. New York, NY, USA: Academic Press, pp. 315-322.
Wodehouse RP (1935). Pollen Grains. New York, NY, USA: McGrawHill. Yıldız B (2012). Cirsium Mill. In: Güner A, Aslan S, Ekim T, Vural M, Babaç. MT (editors). Türkiye Bitkileri Listesi (Damarlı Bitkiler). İstanbul, Turkey: Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği Yayını, pp. 141-146 (in Turkish).
Yıldız B, Arabacı T, Dirmenci T, Çelenk S (2011). Cirsium sivasicum sp. nov. and C. peshmenianum sp. nov. (Asteraceae) and their allies from Turkey. Nord J Bot 29: 26-37.
Yıldız B, Arabacı T, Dirmenci T, Köstekçi S (2016). A taxonomic revision of the genus Cirsium Mill. sect. Cirsium (Asteraceae: Cardueae) in Turkey. Turk J Bot 40: 514-530.
Yüksel E, Kıran Y, Şahin A, Yıldız B, Arabaci T (2013). Karyological studies of 10 Cirsium sect. Epitrachys (Asteraceae) species from Turkey. Turk J Bot 37: 1085-1092.
Zalewska-Gałosz J, Kaplan Z, Kwolek D (2018). Reinterpretation of Potamogeton ×nerviger: solving a taxonomic puzzle after two centuries. Preslia 90: 135-149.