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Molecular study of the Cardamine maritima group (Brassicaceae) from the Balkan and Apennine Peninsulas based on amplified fragment length polymorphism

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Abstract

The amphi-Adriatic region, and especially the Western Balkan Peninsula, belongs to the most important biodiversity hotspots in the temperate region. Nevertheless, detailed phylogeographic and molecular systematic studies in the Western Balkan are rare due to sporadic sampling in regions, where access has been, until recently, restricted by war. The Cardamine maritima group, which is the focus of this study, comprises not only the currently recognised species C. maritima and C. monteluccii, but also other taxa, which have been rendered to synonymy by most of the national floras and checklists. Molecular data acquired by the amplified fragment length polymorphism method showed a clear pattern within the group. Italian populations of C. monteluccii are well separated from Balkan taxa. In a step forward from previous taxonomic confusion surrounding Balkan populations, the present study confirms that five allopatric units—each with a clearly delimited and a rather restricted distribution range—can be easily recognised here. They correspond to C. fialae, C. serbica, C. rupestris, and two genetically distant and allopatric units within C. maritima. While individual taxa gained high bootstrap support in the neighbour-joining tree, there is low support for the internal nodes and it is hard to infer any relationships among taxa based on this information. The majority of Balkan populations of the C. maritima group exhibit features of genetic variability that enable us to hypothesise that these populations are relic ones.

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References

  • Applied Biosystems (1996) AFLPTM plant mapping protocol. PE Applied Biosystems, Foster City

    Google Scholar 

  • Beck GV (1903) Flora Bosne, Hercegovine i Novopazarskog Sandžaka I. Zemaljska Štamparija, Sarajevo

    Google Scholar 

  • Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Molec Ecol 16:3737–3758

    Article  CAS  Google Scholar 

  • Brilli-Cattarini AJB, Gubellini L (1986) Una nuova specie di Cardamine (Cruciferae) dalla Penisola Italiana e Sicilia. Webbia 39:397–407

    Google Scholar 

  • Bussell JD, Waycott M, Chappill JA (2005) Arbitrarily amplified DNA markers as characters for phylogenetic inference. Perspect Pl Ecol Evol Syst 7:3–26

    Article  Google Scholar 

  • Candolle AP (1821) Regni vegetabilis systema naturale 2. Treutel et Würz, Paris

    Google Scholar 

  • Colantoni P, Gallignani P, Lenaz R (1979) Late Pleistocene and Holocene evolution of the North Adriatic continental shelf (Italy). Mar Geol 33:M41–M50

    Article  Google Scholar 

  • Comes PH, Kadereit JW (1998) The effects of quaternary climatic changes on plant distribution and evolution. Trends Pl Sci 3:432–438

    Article  Google Scholar 

  • Corander J, Marttinen P, Sirén J, Tang J (2006) BAPS: Bayesian analysis of population structure, Manual v. 4.1. Available at: http://www.rni.helsinki.fi/-jic/bapspage.html

  • Crisp MD, Laffan S, Linder HP, Monro A (2001) Endemism in the Australian flora. J Biogeogr 28:183–198

    Article  Google Scholar 

  • Dawson AG (1992) Ice age Earth: Late Quaternary geology and climate. Routledge, London

    Google Scholar 

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

    Google Scholar 

  • Eastwood WJ (2004) East Mediterranean vegetation and climatic change. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity—pattern and process in the European hotspot. Kluwer, Dordrecht, pp 25–48

    Google Scholar 

  • Frajman B, Oxelman B (2007) Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Molec Phylogenet Evol 43:140–155

    Article  PubMed  CAS  Google Scholar 

  • Franzke A, Hurka H (2000) Molecular systematics and biogeography of the Cardamine pratensis complex (Brassicaceae). Pl Syst Evol 224:213–234

    Article  CAS  Google Scholar 

  • Fritsch C (1895) Beiträge zur Flora der Balkanhalbinsel mit besonderer Berücksichtigung von Serbien II. Verh K K Zool Bot Ges Wien 44:301–327

    Google Scholar 

  • Fritsch C (1897) Ueber eine neue Cardamine aus der Hercegovina. Österr Bot Z 47:44–46

    Article  Google Scholar 

  • Gömöry D, Paule L, Brus R, Zhelev P, Tomović Z, Gračan J (1999) Genetic differentiation and phylogeny of beech on the Balkan Peninsula. J Evol Biol 12:746–754

    Article  Google Scholar 

  • Guo Y-P, Saukel J, Mittermayr R, Ehrendorfer F (2005) AFLP analyses demonstrate genetic divergence, hybridization, and multiple polyploidization in the evolution of Achillea (Asteraceae-Anthemideae). New Phytol 166:273–290

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez Larena B, Fuertez Aquilar J, Feliner GN (2002) Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Molec Ecol 11:1965–1974

    Article  Google Scholar 

  • Hampe A, Arroyo P, Jordano P, Petit J (2003) Rangewide phylogeography of a bird-dispersed Eurasian shrub: contrasting Mediterranean and temperate glacial refugia. Molec Ecol 12:3415–3426

    Article  CAS  Google Scholar 

  • Hayek A (1927) Prodromus florae peninsulae Balcanicae 1. Verlag des Repertorium, Dahlem bei Berlin

    Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Jalas J, Suominen J (1994) Atlas Florae Europaeae 10. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, Helsinki

    Google Scholar 

  • Jones BMG, Akeroyd JR (1993) 40. Cardamine L. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea 1, 2nd edn. Cambridge University Press, Cambridge, pp 346–351

    Google Scholar 

  • Josifović M (ed) (1972) Flora SR Srbije. Srpska Akademija Nauka u Umetnosti, Beograd

    Google Scholar 

  • Juan A, Crespo MB, Cowan RS, Lexer C, Fay MF (2004) Patterns of variability and gene flow in Medicago citrina, an endangered endemic of island in the western Mediterranean, as revealed by amplified fragment length polymorphism (AFLP). Molec Ecol 13:2679–2690

    Article  CAS  Google Scholar 

  • Koopman WJM (2005) Phylogenetic signal in AFLP data sets. Syst Biol 54:197–217

    Article  PubMed  Google Scholar 

  • Kosman E (2003) Nei’s gene diversity and the index of average differences are identical measures of diversity within populations. Pl Pathol 52:533–535

    Article  Google Scholar 

  • Kryštufek B, Buzan EV, Hutchinson WF, Hänfling B (2007) Phylogeography of the rare Balkan endemic Martino’s vole, Dinaromys bogdanovi, reveals strong differentation within the western Balkan Peninsula. Molec Ecol 16:1221–1232

    Article  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 

  • Kučera J, Lihová J, Marhold K (2006) Taxonomy and phylogeography of Cardamine impatiens and C. pectinata (Brassicaceae). Bot J Linn Soc 152:169–195

    Google Scholar 

  • Lara-Cabrera SI, Spooner DM (2004) Taxonomy of North and Central American diploid wild potato (Solanum sect. Petota) species: AFLP data. Pl Syst Evol 248:129–142

    Article  CAS  Google Scholar 

  • Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–398

    Google Scholar 

  • Lihová J, Marhold K (2006) Phylogenetic and diversity patterns in Cardamine (Brassicaceae)—a genus with conspicuous polyploid and reticulate evolution. In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution, vol. 1C: phanerogams (Angiosperms–Dicotyledons). Science Publishers, Inc., Enfield, pp 149–186

    Google Scholar 

  • 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 

  • Lihová J, Marhold K, Tribsch A, Stuessy TF (2004a) Morphometric and AFLP reevaluation of tetraploid Cardamine amara (Brassicaceae) in the Mediterranean. Syst Bot 29:134–146

    Article  Google Scholar 

  • Lihová J, Tribsch A, Stuessy TF (2004b) Cardamine apennina: a new endemic diploid species of the C. pratensis group (Brassicaceae) from Italy. Pl Syst Evol 245:69–92

    Article  Google Scholar 

  • Lihová J, Shimizu KK, Marhold K (2006) Allopolyploid origin of Cardamine asarifolia (Brassicaceae): incongruence between plastid and nuclear ribosomal DNA sequences solved by a single-copy nuclear gene. Molec Phylogenet Evol 39:759–786

    Article  PubMed  Google Scholar 

  • Marghali S, Panaud O, Lamy F, Ghariani S, Sarr A, Marrakchi M, Trifi-Farah N (2005) Exploration of intra- and inter-population genetic diversity in Hedysarum coronarium L. by AFLP markers. Genet Resour Crop Evol 52:277–284

    Article  CAS  Google Scholar 

  • Médail F, Diadema K (2008) Importance of refugia in shaping plant diversity in the Mediterranean Basin. J Biogeogr (in press)

  • Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nei M, Li W-H (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Nguyen TT, Taylor PW, Redden RJ, Ford R (2004) Genetic diversity estimates in Cicer using AFLP analysis. Pl Breed (New York) 123:173–179

    CAS  Google Scholar 

  • Nikolić T (ed) (1997) Flora Croatica. Index Florae Croaticae. Pars 2. Nat Croat 6(Suppl 1):1–232

  • Pančić J (1884) Dodatak flory Kneževine Srbije. Izdane i štampa kraľ.-srp. Državne štampariji, Beograd

    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 

  • Perný M, Tribsch A, Stuessy TF, Marhold K (2005a) Taxonomy and cytogeography of Cardamine raphanifolia and C. gallaecica (Brassicaceae) in the Iberian Peninsula. Pl Syst Evol 254:69–91

    Article  Google Scholar 

  • Perný M, Tribsch A, Anchev ME (2005b) Infraspecific differentiation in diploid Cardamine acris (Brassicaceae) from Balkan Peninsula: morphological and molecular evidence. Folia Geobot 39:405–429

    Article  Google Scholar 

  • Perný M, Tribsch A, Stuessy T, Marhold K (2005c) Allopolyploid origin of Cardamine silana (Brassicaceae) from Calabria (southern Italy): karyological, morphological and molecular evidence. Bot J Linn Soc 148:101–116

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  PubMed  CAS  Google Scholar 

  • Pignatti S (ed) (1982) Flora d’Italia 1. Edagricole, Bologna

    Google Scholar 

  • Pilon Y, Qamaruz-Zaman F, Fay MF, Hendoux F, Piquot Y (2007) Genetic diversity and ecological differentation in the endangered fen orchid (Liparis loeselii). Conserv Genet 8:177–184

    Article  Google Scholar 

  • Podani J (2001) Syn-Tax 2000, Computer programs for data analysis in ecology and systematics, user′s manual. Scentia Publishing, Budapest

    Google Scholar 

  • Polunin O (1997) Flowers of Greece and the Balkans. Oxford University Press, Oxford

    Google Scholar 

  • Prohens J, Anderson GJ, Blanca JM, Cañizares J, Zuriaga E, Nuez F (2006) The implications of AFLP data for the systematics of the wild species of Solanum section Basarthum. Syst Bot 31:208–216

    Article  Google Scholar 

  • Randi E, Tabarroni C, Rimondi S, Lucchini V, Sfougaris A (2003) Phylogeography of the rock partridge (Alectoris graeca). Molec Ecol 12:2201–2214

    Article  CAS  Google Scholar 

  • Rohlena J (1906) Beitrag zur Flora von Montenegro. Repert Nov Spec Regni Veg 3(36/37):145–149

    Google Scholar 

  • Rohlena J (1942) Conspectus florae Montenegrinae. Preslia 21/22:1–775

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin, vers. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

    Google Scholar 

  • Schönswetter P, Tribsch A (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54:715–732

    Google Scholar 

  • Schulz OE (1903) Monographie der Gattung Cardamine. Bot Jahrb Syst 29:280–623

    Google Scholar 

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

    Article  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford

    Google Scholar 

  • Tribsch A, Schönswetter P, Stuessy TF (2002) Saponaria pumila (Caryophyllaceae) and the ice-age in the Eastern Alps. Amer J Bot 89:2024–2033

    Article  Google Scholar 

  • Trinaistić I (1976) Analitička flora Jugoslavije 2. Institut za Botaniku, Sveučilišta u Zagrebu, Zagreb

    Google Scholar 

  • Turrill WB (1929) The plant life of the Balkan Peninsula: a phytogeographical study. Clarendon Press, Oxford

    Google Scholar 

  • Tzedakis PC (2004) The Balkans as prime glacial refugial territory of European temperate trees. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity-pattern and process in the European hotspot. Kluwer, Dordrecht, pp 49–68

    Google Scholar 

  • Voges A (ed) (1995) International Quaternary map of Europe 1: 2 500 000, B 10 Bern. Bundesanstalt für Geowissenschaften und Rohstoffe/UNESCO, Hannover

    Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Widmer A, Lexer Ch (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16:267–269

    Article  PubMed  Google Scholar 

  • Yeh FC, Yang R-C, Boyle TJ, Ye Z-H, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada

    Google Scholar 

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Acknowledgments

We acknowledge the financial support provided by the Grant Agency VEGA, Bratislava, Slovak Republic (project no. 6055, to Judita Lihová), by the Slovak Research and Development Agency (project no. RPEU-0003-06, to Karol Marhold), by the Ministry of Education, Youth and Sports of the Czech Republic (grant no. 0021620828, to Karol Marhold), and by the Spanish Ministerio de Educación y Ciencia (Juan de la Cierva fellowship, to Karin Tremetsberger). Thanks are also due to J. Lihová (Bratislava, Slovakia) for her useful help and comments on the manuscript, F. Selvi (University of Firenze, Italy), and S. Redžić (from University of Sarajevo, Bosnia and Hercegovina) for their assistance in the field.

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Authors and Affiliations

  1. Institute of Botany, Slovak Academy of Sciences, Dúbravská cesta 14, 845 23, Bratislava, Slovak Republic

    Jaromír Kučera & Karol Marhold

  2. Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes, 41080, Sevilla, Spain

    Karin Tremetsberger

  3. Department of Systematic and Evolutionary Botany, Faculty Center Botany, University of Vienna, Rennweg 14, 1030, Wien, Austria

    Karin Tremetsberger

  4. Department of Botany, Charles University, Benátská 2, 128 01, Praha 2, Czech Republic

    Jaroslav Vojta & Karol Marhold

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  1. Jaromír Kučera
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Correspondence to Karol Marhold.

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Kučera, J., Tremetsberger, K., Vojta, J. et al. Molecular study of the Cardamine maritima group (Brassicaceae) from the Balkan and Apennine Peninsulas based on amplified fragment length polymorphism. Plant Syst Evol 275, 193–207 (2008). https://doi.org/10.1007/s00606-008-0061-8

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