Skip to main content
Log in

Genetic diversity of Tulipa suaveolens (Liliaceae) and its evolutionary relationship with early cultivars of T. gesneriana

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Polychromatic Tulipa suaveolens occurs over a vast territory ranging from the Crimea to eastern Kazakhstan. Its phylogenetic relationship to cultivated T. gesneriana is still under discussion. We used sequences from the psbE–petL region of chloroplast DNA and the complete internal transcribed spacer of nuclear ribosomal DNA to examine the genetic variability of T. suaveolens specimens from European Russia and the adjoining regions. Our data set also included 8 varieties of cultivated T. gesneriana. The research on biogeographic patterns of plastid haplotype and nuclear ribotype distribution provides evidence that their origin and dispersal over the Lower and Middle Volga Region are linked to the Khazar or Early Khvalynian transgression of the Caspian Sea and subsequent events. In the Crimea and the adjacent regions, the pattern of haplotypes’ distribution indicates that their origin and expansion may be linked to the Karangat transgression of the Black Sea and the subsequent New Euxinian regression. Based on our results, we propose that T. suaveolens is the likeliest wild ancestor of early T. gesneriana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abedi R, Babaei A, Karimzadeh G (2015) Karyological and flow cytometric studies of Tulipa (Liliaceae) species from Iran. Pl Syst Evol 301:1473–1484. https://doi.org/10.1007/s00606-014-1164-z

    Article  Google Scholar 

  • Abramova TA (1977) The history of the vegetation cover of the Precaspian in the Late Cenozoic (according to paleobotanical data). Vestn Moskovsk Gosud Univ Ser 5 Geogr 1:74–80 (in Russian)

    Google Scholar 

  • Alvarez I, Wendel JF (2004) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogen Evol 29:417–434. https://doi.org/10.1016/S1055-7903(03)00208-2

    Article  CAS  Google Scholar 

  • Badyukova EN (2007) Age of Khvalynian transgressions in the Caspian Sea region. Oceanology 47:400–405. https://doi.org/10.1134/S0001437007030125

    Article  Google Scholar 

  • Badyukova EN (2015) Istortiya kolebaniy urovnya Kaspiya v pleystotsene (byla li Velikaya Khvalynskaya transgressiya?).  Byull Komiss Izuch Chetvert Perioda 74:111–120 (in Russian)

    Google Scholar 

  • Botschantzeva ZP (1982) Tulips: taxonomy, morphology, cytology, phytogeography and physiology. English edition: trans: Varekamp HQ). Balkema, Rotterdam

  • Bykov BA (1981) Tulipa schrenkii Regel. In: Bykov BA (ed) Red data book of Kazakh SSR, rare and endangered species of animals and plants, part 2: plants. Publishing house “Nauka” of Kazakh SSR, Almaty, pp 31–32 (in Russian)

    Google Scholar 

  • Christenhusz MJM, Govaerts R, David JC, Hall T, Borland K, Roberts PS, Tuomisto A, Buerki S, Chase MW, Fay MF (2013) Tiptoe through the tulips—cultural history, molecular phylogenetics and classification of Tulipa (Liliaceae). Bot J Linn Soc 172:280–328. https://doi.org/10.1111/boj.12061

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659

    Article  CAS  Google Scholar 

  • Clusius C (1601) Rariorum plantarum historia, quae accesserint, proxima pagina docebit, Officina Plantiniana Raphelengii, Antwerp

  • Clusius C (1611) Curae posteriores, seu plurimarum non ante cognitarum, aut descriptarum stirpium, peregrinorumque aliquot animalium novae descriptiones: quibus & omnia ipsius opera, aliaque ab eo versa augentur, aut illustrantur, Officina Plantiniana Raphelengii, Antwerp

  • Cordus V (1561) Annotationes in Pedacii Dioscoridis Anazarbei de Medica materia libros, Strasbourg

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Meth 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  Google Scholar 

  • Dolukhanov PM, Chepalyga AL, Shkatova VK, Lavrentiev NV, Karpinsky AP (2009) Late Quaternary Caspian: sea-levels, environments and human settlement. Open Geogr J 2:1–15. https://doi.org/10.2174/1874923200902010001

    Article  Google Scholar 

  • Dong W, Liu J, Yu J, Wang L, Zhou S (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS ONE 7: e35071. https://doi.org/10.1371/journal.pone.0035071

    Article  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Everett D (2013) The genus Tulipa: tulips of the world. Kew Publishing, Royal Botanic Gardens, Kew

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molec Ecol Resources 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Hall AD (1940) The genus Tulipa. Royal Horticultural Society, London

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hitchcock AS, Green ML (1947) Species lectotypicae generum Linnaei. Brittonia 6:114–118

    Google Scholar 

  • Hoog M (1973) On the origin of Tulipa. In: Napier E, Platt JNO (eds) Lilies and other Liliaceae. Royal Horticultural Society, London, pp 47–64

    Google Scholar 

  • Hurka H, Friesen N, Bernhardt K-G, Neuffer B, Smirnov SV, Shmakov AI, Blattner FR (2019) The Eurasian steppe belt: status quo, origin and evolutionary history. Turczaninowia 22:5–71. https://doi.org/10.14258/turczaninowia.22.3.1

    Article  Google Scholar 

  • Ibadlı OV, Qaraxani PX (2013) Tulipa gesneriana. In: Alakbarov IKh (ed) Red book of the Republic of Azerbaijan, rare and endangered plant and mushroom species, 2nd edn. Şərq-Qərb, Baku, pp 94–95 (in Azerbaijani)

    Google Scholar 

  • Ivaschenko AA (2005) Tulips and other bulbous plants of Kazakhstan. BV Printing House: “Two Kapitals”, Almaty (in Russian)

  • Kashin AS, Kritskaya TA, Schanzer IA (2016a) Genetic polymorphism of Tulipa gesneriana L. evaluated on the basis of the ISSR marking data. Rus J Genet 52:1023–1033. https://doi.org/10.1134/S1022795416100045

    Article  CAS  Google Scholar 

  • Kashin AS, Petrova NA, Shilova IV (2016b) State of cenopopulations and morphological variability of Tulipa gesneriana (Liliaceae) in the northern Lower Volga region. Bot Zhurn (Moscow & Leningrad) 101:1430–1465. https://doi.org/10.1134/S0006813616120061 (in Russian)

    Article  Google Scholar 

  • Kashin AS, Petrova NA, Shilova IV (2017) Some features of the environmental strategy of Tulipa gesneriana L. (Liliaceae, Liliopsida). Biol Bull 44:1237–1245. https://doi.org/10.1134/S1062359017100053

    Article  Google Scholar 

  • Kay K, Whittall JB, Hodges SA (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol 6:36. https://doi.org/10.1186/1471-2148-6-36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirpichnikov AN (2006) Velikiy volzhskiy put’ i mezhdunarodnaya torgovlya i etnokul’turnaya integratsiya v epokhu rannego srednevekov’ya. In: Derevyanko AP, Molodin VI (eds) Sovremennye problemy arkheologii Rossii, part I. Publishing house of the Institute of archeology and ethnography of the SB RAS, Novosibirsk, pp 34–39 (in Russian)

    Google Scholar 

  • Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18:l − 32

    Article  Google Scholar 

  • Kritskaya TA, Kashin AS, Schanzer IA, Danilov VA (2018) Genetic differentiation of Tulipa suaveolens (Liliaceae) in the north-east of its range in the European part of Russia. Bot Zhurn (Moscow & Leningrad) 103:187–201. https://doi.org/10.1134/S0006813618020023 (in Russian)

    Article  Google Scholar 

  • Lan Y, Qu L, Xin H, Gong H, Lei J, Xi M (2018) Physical mapping of rDNA and karyotype analysis in Tulipa sinkiangensis and T. schrenkii. Sci Hort 240:638–644. https://doi.org/10.1016/j.scienta.2018.06.055

    Article  CAS  Google Scholar 

  • Lee C, Wen J (2004) Phylogeny of Panax using chloroplast trnC–trnD intergenic region and the utility of trnC–trnD in interspecific studies of plants. Molec Phylogen Evol 31:894–903. https://doi.org/10.1016/j.ympev.2003.10.009

    Article  CAS  PubMed  Google Scholar 

  • Lepechin II (1771) Dnevnyye zapiski puteshestviya doktora i Akademii nauk ad’yunkta Ivana Lepekhina po raznym provintsiyam Rossiyskogo gosudarstva v 1768 i 1769 godu, part I. Typography of the Imperial Academy of Sciences, St. Petersburg (in Russian)

  • Linnaeus C (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus secundum systema sexuale digestas. L. Salvius, Stockholm

  • Litvinskaya SA (2008) Tulipa schrenkii Regel. In: Trutnev YuP (ed) Red data book of the Russian Federation (plants and fungi). KMK Scientific Press Ltd., Moskow, pp 333–334 (in Russian)

    Google Scholar 

  • Makarov BS (2013) Nederlandse meestertuiniers in Sint-Petersburg in de eerste helft van de 18e eeuw. Nederland-Rusland Centrum, Groningen (in Russian)

    Google Scholar 

  • Marasek-Ciolakowska A, Nishikawa T, Shea DJ, Okazaki K (2018) Breeding of lilies and tulips—interspecific hybridization and genetic background. Breed Sci 68:35–52. https://doi.org/10.1270/jsbbs.17097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mordak EV (1979) Genus Tulipa L. In: Fedorov A (ed) Flora Partis Europaeae URSS [Flora of the USSR], vol. IV. Nauka Publishers, Leningrad, pp 232–236

    Google Scholar 

  • Mordak H (1990) Quid est Tulipa schrenkii Regel et T. heteropetala Ledeb. (Liliaceae)? Novosti Sist Vyssh Rast 27:27–32 (in Russian)

    Google Scholar 

  • Nieto Feliner G, Rossello JA (2007) Better the devil you know? guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molec Phylogen Evol 44:911–919. https://doi.org/10.1016/j.ympev.2007.01.013

    Article  CAS  PubMed  Google Scholar 

  • Pourkhaloee A, Khosh-Khui M, Arens P, Salehi H, Razi H, Niazi A, Afsharifar A, van Tuyl J (2018) Molecular analysis of genetic diversity, population structure, and phylogeny of wild and cultivated tulips (Tulipa L.) by genic microsatellites. Hort Environm Biotechnol 59:875–888. https://doi.org/10.1007/s13580-018-0055-6

    Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Stork A (1984) Tulipes sauvages et cultivées. Conservatoire et jardin botaniques, Geneva

    Google Scholar 

  • Svitoch AA (2008) The Khvalynian transgression of the Caspian Sea and the New-Euxinian basin of the Black Sea. Water Res 35:165–170. https://doi.org/10.1134/S0097807808020048

    Article  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.0 b10. Sinauer, Sunderland

  • Tang N, Shahin A, Bijman P, Liu J, van Tuyl J, Arens P (2013) Genetic diversity and structure in a collection of tulip cultivars assessed by SNP markers. Sci Hort 161:286–292. https://doi.org/10.1016/j.scienta.2013.07.016

    Article  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  Google Scholar 

  • Tkachenko VS (2009) Tulipa schrenkii Regel (~ T. gesneriana L. s.l.). In: YaP Didukha (ed) Chervona kniga Ukraini, rosliny svit. Globalcolsanting, Kiev, p 149 (in Ukrainian)

    Google Scholar 

  • Tudryn A, Chalié F, Lavrushin YuA, Antipov MP, Spiridonova EA, Lavrushin V, Tucholka P, Leroy SAG (2013) Late Quaternary Caspian Sea environment: late Khazarian and Early Khvalynian transgressions from the lower reaches of the Volga River. Quatern Int 292:193–204. https://doi.org/10.1016/j.quaint.2012.10.032

    Article  Google Scholar 

  • Van Raamsdonk LWD (1995) Species relationships and taxonomy in Tulipa subg. Tulipa (Liliaceae). Pl Syst Evol 195:13–44

    Article  Google Scholar 

  • Wen J, Zimmer E (1996) Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Molec Phylogen Evol 6:167–177. https://doi.org/10.1006/mpev.1996.0069

    Article  CAS  PubMed  Google Scholar 

  • Wulff EW (1930) VIII. Tulipa (Tourn.) L. Fl Taurica 1:38–46 (in Russian)

    Google Scholar 

  • Xing G, Qu L, Zhang Y, Xue L, Su J, Lei J (2017) Collection and evaluation of wild tulip (Tulipa spp.) resources in China. Genet Res Crop Evol 64:641–652. https://doi.org/10.1007/s10722-017-0488-2

    Article  Google Scholar 

  • Yanagisawa R, Kuhara T, Nishikawa T, Sochacki D, Marasek-Ciolakowska A, Okazaki K (2012) Phylogenetic analysis of wild and garden tulips using sequences of chloroplast DNA. Acta Hort 953:103–110. https://doi.org/10.17660/ActaHortic.2012.953.14

    Article  Google Scholar 

  • Yanina TA (2014) The Ponto–Caspian region: environmental consequences of climate change during the Late Pleistocene. Quatern Int 345:88–99. https://doi.org/10.1016/j.quaint.2014.01.045

    Article  Google Scholar 

  • Zonneveld BJM (2009) The systematic value of nuclear genome size for “all” species of Tulipa L. (Liliaceae). Pl Syst Evol 281:217–245. https://doi.org/10.1007/s00606-009-0203-7

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The reported study was funded by Russian Fund for Basic Research (RFBR), Project Number 16-04-00142. The authors wish to thank the curators of Herbarium of Lomonosov Moscow State University, especially Aleksey P. Seregin, and the curators of Herbarium of the Royal Botanic Garden Edinburgh, especially Suzanne Cubey, for donation of herbarium specimens. We also thank Nina N. Danilina and Polina S. Klyuchnikova of Tsitsin Main Botanical Garden of Russian Academy of Science for indispensable advice and donation of T. gesneriana cultivars. Our sincere thanks go to Nataly Snegovaya of Institute of Zoology of Azerbaijan National Academy of Sciences for the help in collection of T. julia specimens.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tatyana A. Kritskaya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

The authors comply will all rules of the journal following the COPE guidelines; all authors have contributed and approved the final manuscript.

Additional information

Handling Editor: Ricarda Riina.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Geographic origin, GenBank accession numbers, ITS and cpDNA haplotypes and flower colour in the investigated specimens Tulipa suaveolens.

Online Resource 2. The administrative map of the sampling points of Tulipa suaveolens.

Online Resource 3. Phylogenetic tree resulting from a Bayesian analyses of the cpDNA haplotypes of Tulipa suaveolens. Tulipa julia were used as outgroup taxa.

Online Resource 4. A map of the sampling points and the barriers between the groups of populations of Tulipa suaveolens defined by SAMOVA.

Online Resource 5. Phylogenetic tree resulting from a Bayesian analyses of the ITS sequences of the genus Tulipa. Species from the related genus Erythronium were used as outgroup taxa.

Online Resource 6. Divergence time estimates and ancestral range reconstruction (M1) for the Tulipa suaveolens based on ITS sequences of 19 taxa. Maximum clade credibility tree for divergence times with mean substitution rate according to Kay et al. (2006).

Online Resource 7. Extra large specimens of Tulipa suaveolens found in natural population.

Online Resource 8. Overview photographs of some natural populations of Tulipa suaveolens. Detailed information on each of the populations is available in Online resource 1.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kritskaya, T.A., Kashin, A.S., Perezhogin, Y.V. et al. Genetic diversity of Tulipa suaveolens (Liliaceae) and its evolutionary relationship with early cultivars of T. gesneriana. Plant Syst Evol 306, 33 (2020). https://doi.org/10.1007/s00606-020-01667-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00606-020-01667-7

Keywords

Navigation