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Systematics and evolutionary history of the Asterotricha group of the genus Onosma (Boraginaceae) in central and southern Europe inferred from AFLP and nrDNA ITS data

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Abstract

Onosma is a species-rich genus with complicated patterns of morphological and karyological variation, and controversial taxonomic treatments. In the present study we focused on the Asterotricha group, one of three major infrageneric groups, in the area of central and southern Europe. Ribosomal internal transcribed spacer (ITS) sequences and amplified fragment length polymorphism (AFLP) markers were used to assess species differentiation and relationships, and to gain insight into the evolutionary history of the group. ITS data supported the monophyly of the asterotrichous taxa. Six genetically differentiated entities were resolved by AFLP markers, corresponding to O. echioides, O. heterophylla s.l., O. thracica including O. rigida, O. malkarmayorum, O. taurica, and O. stellulata. Onosma stellulata is identified as the most differentiated lineage within the Asterotricha group, which is consistent with its unique chromosome number. Within O. heterophylla s.l., recognition of O. viridis as a species distinct from O. heterophylla s.str. is supported. On the other hand, O. tornensis appears to be conspecific with O. viridis. Inferring from the patterns of genetic diversity and divergence, the evolutionary history of O. heterophylla s.l. is discussed. Genetic variation within the polymorphic Apennine–Dalmatian O. echioides is almost continuous and shaped by isolation by distance, thus none of the previous intraspecific taxonomic concepts are valid. The assumed hybrid origin of O. malkarmayorum is supported, and its affinity to potential ancestors, O. heterophylla s.l. and O. thracica incl. O. rigida, is indicated. Future studies of asterotrichous Onosma species should focus on diversity centers in the eastern Mediterranean and Asia Minor, to build up a comprehensive taxonomic concept of the group and to clarify its evolution.

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References

  • Albach DC, von Sternburg M, Scalone R, Bardy KE (2009) Phylogenetic analysis and differentiation of Veronica subgenus Stenocarpon in the Balkan Peninsula. Bot J Linn Soc 159:616–636

    Article  Google Scholar 

  • Applied Biosystems (2005) AFLP® plant mapping. Protocol. PE Applied Biosystems, Foster City

  • Ball PW (1972) 9. Onosma L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europea, vol 3. Diapensiaceae to Myoporaceae, Cambridge University Press, Cambridge, pp 89–94

    Google Scholar 

  • Boissier E (1879) Flora Orientalis sive enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum. Vol. IV: Coroliflorae et Monochlamydeae. H. Georg, Genevae & Basileae

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetic studies. Mol Ecol 13:3261–3273

    Article  CAS  PubMed  Google Scholar 

  • Bradley RD, Hillis DM (1997) Recombinant DNA sequences generated by PCR amplification. Mol Biol Evol 14:592–593

    CAS  PubMed  Google Scholar 

  • Cecchi L, Selvi F (2009) Phylogenetic relationships of the monotypic genera Halascya and Paramoltkia and the origins of serpentine adaptation in circummediterranean Lithospermeae (Boraginaceae): insights from ITS and matK DNA sequences. Taxon 58:700–714

    Google Scholar 

  • Chase MW, Hills HG (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220

    Article  Google Scholar 

  • Cohen JI, Davis JI (2009) Nomenclatural changes in Lithospermum (Boraginaceae) and related taxa following a reassessment of phylogenetic relationships. Brittonia 61:101–111

    Google Scholar 

  • Conti F, Abbate G, Alessandrini A, Blasi C (2005) An annotated checklist of the Italian vascular flora. Palombi, Roma

    Google Scholar 

  • Corander J, Marttinen P, Mäntyniemi S (2006) Bayesian identification of stock mixtures from molecular marker data. Fish Bull 104:550–558

    Google Scholar 

  • Cronn R, Cedroni M, Haselkorn T, Grover C, Wendel JF (2002) PCR-mediated recombination in ampliWcation products derived from polyploid cotton. Theor Appl Genet 104:482–489

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Pérez A, Sequeira M, Santos-Guerra A, Catalán P (2008) Multiple colonization, in situ speciation, and volcanism-associated stepping-stone dispersals shaped the phylogeography of the Macaronesian red fescues (Festuca L., Gramineae). Syst Biol 57(5):732–749

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bull Bot Soc Amer 19:11–15

    Google Scholar 

  • Ehrich D (2006) AFLPDAT: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes 6:603–604

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  CAS  PubMed  Google Scholar 

  • Francisco-Ortega J, Fuertes-Aguilar J, Gómez-Campo C, Santos-Guerra A, Jansen RK (1999) Internal transciber spacer sequence phylogeny of Crambe L. (Brassicaceae): molecular data reveal two Old World disjunctions. Mol Phylogenet Evol 11:361–380

    Article  CAS  PubMed  Google Scholar 

  • Frenzel B, Pesci B, Velichko AA (1992) Atlas of palaeoclimates and palaeoenvironments of the Northern Hemisphere. Geographical Research Institute, Hungarian Academy of Sciences & Fischer, Budapest and Stutgart

  • Fuertes Aguilar J, Nieto Feliner G (2003) Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae). Mol Phylogenet Evol 28:430–447

    Article  CAS  PubMed  Google Scholar 

  • Greuter W, Burdet HM, Long G (1984) Med-Checklist, 1. Conservatoire Botanique de Genève, Genève and Berlin

  • Grinţescu I, Nyárády EI (1969) Genul 403. Onósma L. In: Săvulescu T (ed) Flora republicii populare Romîne. Publishing house of the Romanian Academy of Sciences, Bucharest, pp 214–227

    Google Scholar 

  • Háberová I, Karasová E (1994) Ochrana rastlinstva. In: Rozložník M, Karasová E (eds) Slovenský kras, Chránená krajinná oblast’—biosférická rezervácia. Martin, Osveta, pp 375–391

    Google Scholar 

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

    CAS  Google Scholar 

  • Hedrén M, Fay MF, Chase MW (2001) Amplified fragment length polymorphism (AFLP) reveal details of polyploid evolution in Dactylorhiza (Orchidaceae). Am J Bot 88:1868–1880

    Article  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Qaternary. Philos Trans R Soc B 359:183–195

    Article  CAS  Google Scholar 

  • Holub J (1999) Onosma tornensis Jávorka. In: Čeřovský J, Feráková V, Holub J, Maglocký Š, Procházka F (eds) Červená kniha ohrozených a vzácnych druhov rastlín a živočíchov SR a ČR, vol 5. Vyššie rastliny. Príroda, Bratislava, p 257

    Google Scholar 

  • Holub J, Kmet’ová E (1993) 4. Onosma L. Rumenica. In: Bertová L, Goliašová K (eds) Flóra Slovenska V/1. Veda, Bratislava, pp 32–41

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayasian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaudoise Sci Nat 44:223–270

    Google Scholar 

  • Jakucs P (1952) Ujaob adatok a Tornense flórájához. Ann Biol Univ Hung 2:235–243

    Google Scholar 

  • Jávorka S (1906) Hazai Onosma-fajink. Ann Hist Natur Mus Natl Hung 4:406–449

    Google Scholar 

  • Johnston IM (1954) Studies in the Boraginaceae, XXVI. Further evaluations of the genera of the Lithospermeae. J Arnold Arbor 35:1–81

    Google Scholar 

  • Karasová E (1994) Osobitne chránené územia. In: Rozložník M, Karasová E (eds) Slovenský kras, Chránená krajinná oblast’–biosférická rezervácia. Osveta, Martin, pp 418–432

    Google Scholar 

  • Klokov MV, Dobroczaeva DM (1957) Rid 690. Gromovik–Onosma L. In: Kotov MI, Barbarič AI (eds) Flora URSR, Tom VIII. Public House of the Ukrainian Academy of Sciences, Kiev, pp 351–377

    Google Scholar 

  • Kolarčik V, Mártonfi P (2006) Revision of the distribution of the genus Onosma (Boraginaceae) in Slovakia. Thaiszia–J Bot Košice 16:131–154

    Google Scholar 

  • Kováts D (1975) Boraginaceae type specimens of Herbarium Carpato-Pannonicum. Studia Bot Hung 10:123–132

    Google Scholar 

  • Kryštufek B, Reed JM (2004) Pattern and process in Balkan biodiversity―an overview. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity―pattern and process in the European hotspot. Kluwer, Dordrecht, pp 1–8

    Google Scholar 

  • Krzanowski WJ (1990) Principles of multivariate analysis. Clarendon, Oxford

    Google Scholar 

  • Kučera J, Marhold K, Lihová J (2010) Cardamine maritima group (Brassicaceae) in the amphi-Adriatic area: A hotspot of species diversity revealed by DNA sequences and morphological variation. Taxon 59:148–164

    Google Scholar 

  • Lacaita C (1924a) Piante italiane critiche o rare (XCI–XCVII). Nuovo Giorn Bot Ital, serie 2 31:18–35

    Google Scholar 

  • Lacaita C (1924b) The Onosmas of Linnaeus and Sibthorp, with a note on those of Tournefort’s Herbarium. J Linn Soc Bot 46:387–400

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

  • Lihová J, Tribsch A, Marhold K (2003) The Cardamine pratensis (Brassicaceae) group in the Iberian Peninsula: taxonomy, polyploidy and distribution. Taxon 52:783–802

    Article  Google Scholar 

  • Logacheva MD, Valiejo-Roman CM, Pimenov MG (2008) ITS phylogeny of West Asian Heracleum species and related taxa of Umbelliferae-Tordylieae W.D.J.Koch, with notes on evolution of their psbA-trnH sequences. Pl Syst Evol 270:139–157

    Article  CAS  Google Scholar 

  • Luque T (1990) Karyological studies on Spanish Boraginaceae. V: Onosma L., Cerinthe L. and Alkanna Tausch (Lithospermae). Bot J Linn Soc 102:261–272

    Article  Google Scholar 

  • Mansion G, Selvi F, Guggisberg A, Conti E (2009) Origin of Mediterranean insular endemics in Boraginales: integrative evidence from molecular dating and ancestral area reconstruction. J Biogeogr 36:1282–1296

    Article  Google Scholar 

  • Mártonfi P, Mártonfiová L, Kolarčik V (2008) Karyotypes and genome size of Onosma species from northern limits of the genus in Carpathians. Caryologia 61:363–374

    Google Scholar 

  • Mengoni A, Gonelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random amplified polymorphic DNA analysis. Mol Ecol 9:1319–1324

    Article  CAS  PubMed  Google Scholar 

  • Mengoni A, Selvi F, Cusimano N, Galardi F, Gonnelli C (2006) Genetic diversity inferred from AFLP fingerprinting in populations of Onosma echioides (Boraginaceae) from serpentine and calcareous soils. Pl Biosystems 140:211–219

    Article  Google Scholar 

  • Mered’a P, Hodálová I, Šefer J, Lasák R, Dítě D, Kubandová M, Feráková V, Kubínska A, Marhold K (2005) Hodnotenie stavu zachovalosti populácií anexových druhov rastlín na Slovensku z hľadiska ich ochrany. In: Polák P, Saxa A (eds) Priaznivý stav biotopov a druhov európskeho významu. Štátna ochrana prírody Slovenskej republiky, Banská Bystrica, pp 246–330

    Google Scholar 

  • Mered’a P, Hodálová I, Mártonfi P, Kučera J, Lihová J (2008) Intraspecific variation in Viola suavis in Europe: parallel evolution of white-flowered morphotypes. Ann Bot 102:443–462

    Article  Google Scholar 

  • Meusel H, Jäger E, Rauschert S, Weinert E (1978) Vergleichende Chorologie der zentraleuropäischen Flora -Karten-Band II. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Mráz P (2004) Chorologické a ekologické poznámky ku komplexu Campanula rotundifolia a k druhu Campanula carpatica. Bull Slov Bot Spoločn Bratislava 26:129–135

    Google Scholar 

  • Murín A (1960) Substitution of cellophane for glass covers to facilitate preparation of permanent squashes and smears. Stain Technol 35:351–353

    PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 76:5269–5273

    Article  CAS  PubMed  Google Scholar 

  • Oprea A (2005) Lista critică a plantelor vasculare din România. Publishing House of the Alexandru Ioan Cuza University, Iaşi

    Google Scholar 

  • Park J-M, Kovačić S, Liber Z, Eddie WMM, Schneeweiss GM (2006) Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. Syst Bot 31:862–880

    Article  Google Scholar 

  • Pavlova D (2009) Onosma bulgarica sp. nov. (Boraginaceae–Lithospermeae) found on serpentine in Bulgaria. Nordic J Bot 27:216–221

    Article  Google Scholar 

  • Peruzzi L, Passalacqua NG (2008) Taxonomy of the Onosma echioides (L.) L. complex (Boraginaceae) based on morphometric analysis. Bot J Linn Soc 157:763–774

    Article  Google Scholar 

  • Petrova A (1989) Onosma L. In: Jordanov D (ed) Flora Reipublicae Popularis Bulgaricae IX. Publishing House of the Bulgarian Academy of Sciences, Sofia, pp 126–134

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Rauscher JT, Doyle JJ, Brown HD (2002) Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex. Mol Ecol 11:2691–2702

    Article  CAS  PubMed  Google Scholar 

  • Rauschert S (1976) Zur Nomenklatur und Chorologie des Formenkreises von Onosma pseudoarenarium Schur s. lat. Folia Geobot Phytotax 11:269–279

    Google Scholar 

  • Riedl H (1978) 22. Onosma L. In: Davis PH (ed) Flora of Turkey and the Aegean Islands, vol 6. Edinburgh University Press, Edinburgh, pp 326–376

    Google Scholar 

  • Schlüter PM, Harris SA (2006) Analysis of multilocus fingerprinting data sets containing missing data. Mol Ecol Notes 6:569–572

    Article  Google Scholar 

  • Schönswetter P, Tribsch A (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L (Apiaceae). Taxon 54:725–732

    Article  Google Scholar 

  • Selvi F, Cecchi L, Coppi A (2009) Phylogeny, karyotype evolution and taxonomy of Cerinthe L. (Boraginaceae). Taxon 58:1307–1325

    Google Scholar 

  • Stefanović S, Lakušić D, Kuzmina M, Međedović S, Tan K, Stevanović V (2008) Molecular phylogeny of Edraianthus (Grassy Bells; Campanulaceae) based on non-coding plastid DNA sequences. Taxon 57:452–475

    Google Scholar 

  • Stehlik I, Schneller JJ, Bachmann K (2002) Imigration and in situ glacial survival of the low-alpine Erinus alpinus (Scrophulariaceae). Biol J Linn Soc 77:87–103

    Article  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland, MA, USA

    Google Scholar 

  • Tan K, Petrova A (2009) Nomenclatural notes. Phytol Balcan 15:291–292

    Google Scholar 

  • Tatar M (1938) A pannóniai flora endémikus fajai. Acta Geobot Hung 2:63–127

    Google Scholar 

  • Teppner H (1971) Cytosystematik, bimodale Chromosomensätze und permanente Anorthoploidie bei Onosma (Boraginaceae). Österr Bot Z 119:196–233

    Article  Google Scholar 

  • Teppner H (1972) Cytosystematische Studien an Onosma (Boraginaceae). Ber Deutsch Bot Ges 84:691–696

    Google Scholar 

  • Teppner H (1974) Karyosystematik einiger asiatischer Onosma-Arten (Boraginaceae), inkl. O. inexspectatum Teppner, spec. nov. Pl Syst Evol 123:61–82

    Article  Google Scholar 

  • Teppner H (1981) Karyosystematik von Onosma stellulatum, O. pygmaeum und O. leptanthum (Boraginaceae). Bot Jahrb Syst 102:297–306

    Google Scholar 

  • Teppner H (1982) Onosma L. In: Pignatti S (ed) Flora d’Italia, 2. Bologna, Edagricole, pp 400–402

    Google Scholar 

  • Teppner H (1991a) Onosma L. In: Strid A, Tan K (eds) Mountain Flora of Greece, 2. University Press, Edinburgh, pp 25–38

    Google Scholar 

  • Teppner H (1991b) Karyology of some Greek Onosma species (Boraginaceae). Bot Chron 10:271–292

    Google Scholar 

  • Teppner H (1996a) Die Onosma-Arten (Boraginaceae-Lithospermeae). Rumäniens Stapfia 45:47–54

    Google Scholar 

  • Teppner H (1996b) Blüten und Blütenbesucher bei Onosma (Boraginaceae–Lithospermeae). Feddes Repert 106:525–532

    Article  Google Scholar 

  • Teppner H (2008) An asterotrichous, hexaploid Onosma from Bulgaria: O. malkarmayorum spec. nova (Boraginaceae-Lithospermeae). Phyton (Horn) 48:117–132

    Google Scholar 

  • Thomas DC, Weigend M, Hilger HH (2008) Phylogeny and systematics of Lithodora (Boraginaceae-Lithospermeae) and its affinities to the monotypic genera Neatostema, Mairetis, Halacsya and Paramoltkia based on ITS1 and trnLUAA-sequence data and morphology. Taxon 57:79–97

    Google Scholar 

  • Velenovský J (1895) Flora Bulgarica. Descriptio et enumeratio systematica plantarum vascularum in principatu bulgariae sponte nascentium. Supplementum I. F. Řivnáč, Prague

  • Vos P, Hogers R, Bleeker R, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414

    Article  CAS  PubMed  Google Scholar 

  • Vouillamoz J (2001) Approches cytotaxonomique et moléculaire de la phylogéographie des taxons du genre Onosma (Boraginaceae) en Suisse et dans les pays limitrophes. PhD thesis [depon. in Faculté des Sciences de l′Université de Lausanne, Lausanne]

  • Weigend M, Gottsschling M, Selvi F, Hilger HH (2009) Marbleseeds are gromwells–Systematics and evolution of Lithospermum and allies (Boraginaceae tribe Lithospermeae) based on molecular and morphological data. Mol Phylogenet Evol 52:755–768

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Mária Čudejková, Emília Karasová, Marcus A. Koch, Filippo Maggi, L’uboš Majeský, Karol Marhold, Patrik Mráz, Gavril Negrean, Marián Perný, Helena Rosinová, Emília Sasáková, Alžbeta Szabóová, Stanislav Španiel, and Róbert Šuvada for assistance in plant material sampling and for technical help. We would also like to thank Nicodemo G. Passalacqua and Federico Selvi for useful information on some localities in Italy, Alessio Mengoni for the consultation on DNA isolation protocol, and Kateřina Svoboda and John Brooker for improving the English of the manuscript. We are grateful to anonymous reviewers for helpful comments on the manuscript. Finally, the Ministry of Environment of the Slovak Republic is also acknowledged for gently providing exception from nature conservation of Ministry of Environment of the Slovak Republic no. 1210/481/05-5.1, which allowed us to collect plant material in Slovakia. Support for this research was provided by the Grant Agency for Science, Bratislava (VEGA, No. 1/0012/08) and by the Slovak Research and Development Agency, Bratislava (APVV, No. 51-026404).

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  1. Institute of Botany, Slovak Academy of Sciences, Dúbravská cesta 9, 845 23, Bratislava, Slovak Republic

    V. Kolarčik & J. Zozomová-Lihová

  2. Institute of Biology and Ecology, Faculty of Science, P. J. Šafárik University, Mánesova 23, 041 54, Košice, Slovak Republic

    V. Kolarčik & P. Mártonfi

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Kolarčik, V., Zozomová-Lihová, J. & Mártonfi, P. Systematics and evolutionary history of the Asterotricha group of the genus Onosma (Boraginaceae) in central and southern Europe inferred from AFLP and nrDNA ITS data. Plant Syst Evol 290, 21–45 (2010). https://doi.org/10.1007/s00606-010-0346-6

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