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Morphological variation, genetic diversity and genome size of critically endangered Haberlea (Gesneriaceae) populations in Bulgaria do not support the recognition of two different species

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Abstract

Haberlea is one of the few Gesneriaceae genera that has entered Europe. It is a highly endangered genus and red-listed in Bulgaria. Two species, H. rhodopensis and H. ferdinandi-coburgii, have been described to occur in Bulgaria, but this has never been addressed systematically. Here, we used molecular ISSR markers, morphological and nuclear DNA content to investigate the taxonomic and genetic status of Haberlea in Bulgaria. We found low levels of genetic diversity but significant genetic differentiation among the 12 investigated populations, with a strong separation between Balkan Mountain populations in the north and Rhodope Mountain populations in the south. However, the multivariate morphological analyses did not support such a division. The population from near Lovech, the type locality of the putative species H. ferdinandi-coburgii, did not differ in ploidy level from H. rhodopensis and did not form a separate entity in neither of the analyses and the existence of this species is therefore not supported.

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References

  • Adamović L (1903) On Urumoff’s Haberlea ferdinandi-coburgii. Bot Centralbl 92(24):207

    Google Scholar 

  • Archibald JK, Mort ME, Crawford DJ, Santos-Guerra A (2006) Evolutionary relationships within recently radiated taxa: comments on methodology and analysis of inter-simple sequence repeat data and other hypervariable, dominant markers. Taxon 55:747–756

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Bazos I, Petrova A (2010) Haberlea rhodopensis. In: IUCN 2011 IUCN red list of threatened species, version 2011.1

  • Beaufort-Murphy HT (1983) The seed surface morphology of the Gesneriaceae utilizing the scanning electron microscope and a new system for diagnosing seed morphology. Selbyana 6:220–422

    Google Scholar 

  • Biodiversity Law (2002) Decree N283 accepted by the National Assembly. Darzhaven Vestnik, N77/09.08.2002:9–42 (in Bulgarian)

  • Biserkov V (2011) Red data book of the Republic of Bulgaria, vol 3. Natural habitats. Joint edition of the Bulgarian Academy of Sciences and Ministry of Environment and Water http://e-ecodb.bas.bg/rdb/en/vol3/

  • Borhidi A (1968) Karyological studies on southeast European plant species, I. Acta Botanica Academiae Scientarium Hungaricae 14:253–260

    Google Scholar 

  • Burtt BL (1977) Classification above the genus, as exemplified by Gesneriaceae, with parallels from other groups. Pl Syst Evol Suppl 1:97–109

    Google Scholar 

  • Burtt BL (1997) Old World Gesneriaceae: V. Suprageneric names. Edinb J Bot 54:85–90

    Article  Google Scholar 

  • Camacho FJ, Liston A (2001) Population structure and genetic diversity of Botrychium pumicola (Ophioglossaceae) based on inter-simple sequence repeats (ISSR). Amer J Bot 88:1065–1070

    Article  CAS  Google Scholar 

  • Casgrain P, Legendre P, Vaudor A (2005) The Royal package for multivariate and spatial analysis, Version 4.0 (development release 10)

  • Cattell RB (1966) The scree test for the number of factors. Multivar Behav Res 1:245–276

    Article  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    Article  CAS  PubMed  Google Scholar 

  • Contandriopoulos J (1966) Contribution á l’étude caryologiques des Gesnériacées d’Europe et de leur germination. 91 Congrès des Sociétés Savantes. Rennes 3:271–280

    Google Scholar 

  • Costich DE, Ortiz R, Meagher RT, Bruederle LP, Vorsa N (1993) Determination of ploidy level and nuclear DNA content in blueberry by flow cytometry. Theor Appl Genet 86:1001–1006

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA mini-preparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Doležel J, Bartoš J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110

    Article  PubMed  Google Scholar 

  • Dubreuil M, Riba M, Mayol M (2008) Genetic structure and diversity in Ramonda myconi (Gesneriaceae): effects of historical climate change on a preglacial relict species. Amer J Bot 95:577–587

    Article  CAS  Google Scholar 

  • Eckert JE (1933) The flight range of the honeybee. J Agricult Res 47:257–285

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Fang DQ, Roose ML (1997) Identification of closely related citrus cultivars with inter-simple sequence repeat genetics. Theor Appl Genet 95:408–417

    Article  CAS  Google Scholar 

  • Frivaldszky I (1835) Közlések a’ Balkány’ vidékén tett természettudományi utazásról. Magyar Tud Társ Évk 2:235–276

    Google Scholar 

  • Ganchev I (1950) Anabiotic desiccation resistance and other biological traits of Haberlea rhodopensis Friv. Rep Inst Bot Bulg Acad Sci 1(1):191–214

    Google Scholar 

  • Gao LM, Möller M, Zhang XM, Hollingsworth ML, Liu J, Mill RR, Gibby M, Li DZ (2007) High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam. Mol Ecol 16:4684–4698

    Article  CAS  PubMed  Google Scholar 

  • Greilhuber J (2005) Intraspecific variation in genome size in angiosperms: identifying its existence. Ann Bot 95:91–98

    Article  CAS  PubMed  Google Scholar 

  • Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown ADH, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer, Sunderland, pp 43–63

    Google Scholar 

  • Hogbin PM, Peakall R (1999) Evaluation of the contribution of genetic research to the management of the endangered plant Zieria prostrata. Conserv Biol 13:514–522

    Article  Google Scholar 

  • Huff DR, Peakall R, Smouse PE (1993) RAPD variation within and among natural populations of outcrossing buffalograss. Theor Appl Genet 86:927–934

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Kiani M, Memariani F, Zarghami H (2012) Molecular analysis of species of Tulipa L. from Iran based on ISSR markers. Plant Syst Evol 298:1515–1522

    Article  CAS  Google Scholar 

  • Leitch I, Bennett M (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476

    Article  Google Scholar 

  • Lepper L (1970) Beiträge zur Chromosomenzahlen-Dokumentation. Wissenschaftliche Zeitschrift Friedrich-Schiller-Universität Jena/Thüringen. Mathematisch-naturwissenschaftliche Reihe 19:369–376

  • Markova M (1995) Semeistvo CXX. Silivryakovi–Gesneriaceae Dum. [Gesneria family—Gesneriaceae Dum.]. In: Kozhuharov S (ed) Flora Reipubl. Bulgaricae, Editio Acad. “Prof. Marin Drinov”, Serdicae. pp 288–291

  • Milne C (1975) Chromosome numbers in the Gesneriaceae: V. Notes Roy. Bot Gard Edinb 33:523–525

    Google Scholar 

  • Möller M, Gao LM, Mill RR, Li DZ, Hollingsworth ML, Gibby M (2007) Morphometric analysis of the Taxus wallichiana complex (Taxaceae) based on herbarium material. Bot J Lin Soc 155(3):307–335

    Article  Google Scholar 

  • Munthali M, Ford-Lloyd BV, Newbury HJ (1992) The random amplification of polymorphic DNA for fingerprinting plants. PCR Meth Applic 1:274–276

    Article  CAS  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Amer Nat 106:283–392

    Article  Google Scholar 

  • Obermayer R, Leitch IL, Hanson L, Bennett M (2002) Nuclear DNA C-values in 30 species double the familial representation in pteridophytes. Ann Bot 90:209–217

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics doi:10.1093/bioinformatics/bts460

  • Petrova A (2006) Atlas of Bulgarian endemic plants. Gea-Libris Publishing House, Sofia

    Google Scholar 

  • Petrova A, Vladimirov V (2010) Balkan endemics in the Bulgarian flora. Phytol Balcan 16:293–311

    Google Scholar 

  • Petrova G, Tosheva A, Mladenov P, Moyankova D, Djilianov D (2010) Ex situ collection of model resurrection plant Haberlea rhodopensis as a prerequisite for a biodiversity and conservation studies. Biotechnol & Biotechnol Eq 24:1955–1959

    Article  Google Scholar 

  • Ratnieks FLW (2000) How far do bees forage. Bee Improv 6:10–11

    Google Scholar 

  • Siljak-Yakovlev S, Stevanovic V, Tomasevic M, Brown SC, Stevanovic B (2008) Genome size variation and polyploidy in the resurrection plant genus Ramonda: cytogeography of living fossils. Environm Exp Bot 62:101–112

    Article  CAS  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy—the principles and practice of numerical classification. WH Freeman, San Francisco

    Google Scholar 

  • Strid A (1991) Haberlea rhodopensis Friv. In: Strid A, Tan K (eds) Mountain flora of Greece, vol 2. Edinburgh University Press, Edinburgh, p 260

    Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Szeląg Z, Somlyay L (2009) History of typification of Haberlea rhodopensis Friv. (Gesneriaceae). Ann Bot Fenn 46:555–558

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Turrill WB (1951) Some problems of plant range and distribution. J Ecol 39:205–227

    Article  Google Scholar 

  • Urumoff IK (1902) Plantae novae bulgaricae. Period Spis Bulg Knizh Druzh 63:573

    Google Scholar 

  • Vassilev P (1984) Haberlea rhodopensis Friv. In: Velchev V (ed) Red data book of the PR Bulgaria, vol 1. 349, Plants. Publishing House Bulgarian Academy of Sciences, Sofia

  • Voglmayr H (2000) Nuclear DNA amounts in mosses (Musci). Ann Bot 85:531–546

    Article  CAS  Google Scholar 

  • Vokou D, Petandiou Th, Bellos D (1990) Pollination ecology and reproductive potential of Jancaea heldreichii (Gesneriaceae); a tertiary relict on Mt Olympus, Greece. Biol Cons 52:125–133

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Lee TV, 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 

  • Walter KS, Gillet HJ (1998) Red list of threatened plants compiled by the World Conservation Monitoring Centre, IUCN. The World Conservation Union, Gland, Switzerland and Cambridge, UK

  • Weber A (2004) Gesneriaceae. In: Kubitzki K, Kadereit JW (ed) The families and genera of vascular plants, Dicotyledons. Lamiales (except Acanthaceae incl. Avicenniaceae), vol 7. Springer, Berlin, pp 63–158

  • Weber A, Skog LE (2007) The genera of Gesneriaceae. Basic information with illustration of selected species. http://www.generagesneriaceae.at

  • Wolfe AD, Liston A (1998) Contributions of PCR-based methods to plant systematics and evolutionary biology. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants: DNA sequencing. Kluwer, New York, pp 43–86

    Google Scholar 

  • Wolfe AD, Randle CP (2001) Relationships within and among species of the holoparasitic genus Hyobanche (Orobanchaceae) inferred from ISSR banding patterns and nucleotide sequences. Syst Bot 26:120–130

    Google Scholar 

  • Xiao LQ, Gong X (2006) Genetic differentiation and relationship of populations in Cycas balansae complex (Cycadaceae) and its conservation implications. Ann Bot 97:807–812

    Article  CAS  PubMed  Google Scholar 

  • Zietkiewicz E, Rafalski A, Labuda D (1994) Genome fingerprinting by simple sequence repeats (SSR)-anchored PCR amplifications. Genomics 20:176–183

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We like to thank Petko Mladenov from the Abiotic Stress Group (ABI), and Dr. Anita Tosheva, Department of Botany, Faculty of Biology, Sofia University, for support in the collection of study material. We like to thank the European Commission for a FPVI European-funded Integrated Infrastructure Initiative SYNTHESYS grant to DM (GB-TAF-4741). The Royal Botanic Garden Edinburgh (RBGE) is supported by the Rural and Environment Science and Analytical Services division (RESAS) in the Scottish Government.

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  1. Agrobioinstitute, 8 Draghan Tsankov Blvd, 1164, Sofia, Bulgaria

    Galya Petrova, Teodora Dzhambazova, Daniela Moyankova, Desislava Georgieva & Dimitar Djilianov

  2. Laboratory of Haematopathology and Immunology, National Specialized Hospital for Active Treatment of Haematological Diseases, Sofia, Bulgaria

    Antoaneta Michova

  3. Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, Scotland, UK

    Michael Möller

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  1. Galya Petrova
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  2. Teodora Dzhambazova
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  3. Daniela Moyankova
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  4. Desislava Georgieva
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  5. Antoaneta Michova
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  6. Dimitar Djilianov
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  7. Michael Möller
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Correspondence to Dimitar Djilianov or Michael Möller.

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G. Petrova and M. Möller contributed equally to the work and should be considered first authors.

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Petrova, G., Dzhambazova, T., Moyankova, D. et al. Morphological variation, genetic diversity and genome size of critically endangered Haberlea (Gesneriaceae) populations in Bulgaria do not support the recognition of two different species. Plant Syst Evol 300, 29–41 (2014). https://doi.org/10.1007/s00606-013-0857-z

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