Skip to main content

Advertisement

Log in

Genetic Variation in Three Closely Related Minuartia (Caryophyllaceae) Species Endemic to Greece: Implications for Conservation Management

  • Published:
Folia Geobotanica Aims and scope Submit manuscript

Abstract

The genus Minuartia is highly diverse in the Mediterranean region and includes several endemic and locally restricted species. The genetic variation of three Minuartia species (M. dirphya, M. parnonia, M. wettsteinii) which are endemic to Greece was investigated, aiming to also develop effective conservation plans for their protection. Minuartia dirphya and M. wettsteinii are known to occur only at their type localities, each forming a small population, while M. parnonia is more widespread with seven populations located in the south-east Peloponnese. Genetic diversity was estimated using ten chloroplast microsatellite and five REMAP markers. The chloroplast microsatellite markers exhibited limited polymorphism among species only, while REMAP revealed a significant amount of genetic variation at the population and species level. All the analyses performed (dendrograms, PCoA, STRUCTURE) showed clear differentiation among species, highlighting M. wettsteinii as the most genetically distant. As shown by AMOVA, a degree of differentiation was detected within M. parnonia, where 41 % of the total variation was partitioned among populations and 59 % to the individuals within them. At the species level, the highest genetic diversity (PPB = 75.86 %, Hj = 0.2728, I = 0.3509) was observed in M. parnonia, followed by M. dirphya (PPB = 55.17 %, Hj = 0.2350, I = 0.2767), while the lowest was observed in M. wettsteinii (PPB = 28.74 %, Hj = 0.1449, I = 0.1498). Scarce gene flow (N m = 0.5451) was observed among M. parnonia populations. The current study is important for developing conservation management plans for the three threatened Minuartia species.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Batista F, Banares A, Caujapé-Castells J, Carque E, Marrero-Gómez M, Sosa PA (2001) Allozyme diversity in three endemic species of Cistus (Cistaceae) from the Canary Islands: intraspecific and interspecific comparisons and implications for genetic conservation. Am J Bot 88:1582–1592

  • Baumel A, Ainouche ML, Kalendar R, Schulman AH (2002) Retrotransposons and genomic stability in populations of the young allopolyploid species Spartina anglica C.E. Hubbard (Poaceae). Mol Biol Evol 19:1218–1227

    Article  CAS  PubMed  Google Scholar 

  • Biswas MK, Xu Q, Deng XX (2010) Utility of RAPD, ISSR, IRAP and REMAP markers for the genetic analysis of Citrus spp. Sci Hort 124:254–261

    Article  CAS  Google Scholar 

  • Bittrich V (1993) Caryophyllaceae. In Kubitzki K, Rohwer JG, Bittrich V (eds) The Families and Genera of Vascular Plants, vol. 2, Flowering Plants Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families. Springer, Germany, pp 206–236

    Google Scholar 

  • Boronnikova SV, Kalendar RN (2010) Using IRAP markers for analysis of genetic variability in populations of resource and rare species of plants. Russ J Genet 46(1):36–42

    Article  CAS  Google Scholar 

  • Branco JSC, Vieira EA, Malone G, Kopp MM, Malone E, Bernardes A, Mistura CC, Carvalho FIF, Oliveira CA (2007) IRAP and REMAP assessments of genetic similarity in rice. J Appl Genet 48:107–113

    Article  PubMed  Google Scholar 

  • Bryan GJ, McNicoll J, Ramsay G, Meyer RC (1999) Polymorphic simple sequence repeat markers in chloroplast genomes of Solanceous plants. Theor Appl Genet 99:859–867

    Article  CAS  Google Scholar 

  • Carvalho A, Guedes-Pinto H, Martins-Lopes P, Lima-Brito J (2010) Genetic variability of Old Portuguese bread wheat cultivars assayed by IRAP and REMAP markers. Ann Appl Biol 156:337–345

    Article  CAS  Google Scholar 

  • Coart E, Van Glabeke S, Petit RJ, Van Bockstaele E, Roldán-Ruiz I (2005) Range wide versus local patterns of genetic diversity in hornbeam (Carpinus betulus L.). Conserv Genet 6:259–273

    Article  CAS  Google Scholar 

  • Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438

    Article  Google Scholar 

  • Dan T, Ikeda H, Mitsui Y, Isagi Y, Setoguchi H (2009) Genetic structure of refugial populations of the temperate plant Shortia rotundifolia (Diapensiaceae) on a subtropical island. Conserv Genet 10:859–867

    Article  CAS  Google Scholar 

  • De Montmollin B, Strahm W (eds) (2005) The Top 50 Mediterranean Island Plants: Wild plants at the brink of extinction, and what is needed to save them. IUCN/SSC Mediterranean Islands Plant Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK. x+110 pp

  • DOnofrio C, De Lorenzis G, Giordani T, Natali L, Cavallini A, Scalabrelli G. (2010) Retrotransposon-based molecular markers for grapevine species and cultivars identification. Tree Genet Genomes 6:451–466

    Article  Google Scholar 

  • Doulaty Baneh H, Mohammadi SA, Labra M, Nazemieh A, De Mattia F, Mardi (2007) Chloroplast Microsatellites Markers to Assess Genetic Diversity in Wild and Cultivated Grapevines of Iran. Pak J Biol Sci 10:1855–1859

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus 12:13–15

    Google Scholar 

  • Ducousso A, Petit D, Valero M, Vernet P (1990) Genetic variation between and within populations of a perennial grass: Arrhenatherum elatius. Heredity 65:179–188

    Article  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    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 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Frankham R, Ballou, JD, Briscoe DA (2010) Introduction to conservation genetics. 2nd Ed, Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gautschi B, Widmer A, Joshi J, Koella JC (2002) Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tesellata. Conserv Genet 3:235–245

    Article  CAS  Google Scholar 

  • Ge XJ, Yu Y, Yuan YM, Huang HW, Yan C (2005) Genetic diversity and geographic differentiation in endangered Ammopiptanthus (Leguminosae) populations in desert regions of Northwest china as revealed by ISSR analysis. Ann Bot-London 95:843–851

    Article  CAS  Google Scholar 

  • Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792

    Article  CAS  PubMed  Google Scholar 

  • Godt MJW, Johnson BR, Hamrick JL (1996) Genetic diversity and population size in four rare southern Appalachian plant species. Conserv Biol 10:796–805

    Article  Google Scholar 

  • Godt MJW, Walker J, Hamrick JL (1997) Genetic diversity in the endangered lily Harperocallis flava and a close relative, Tofieldia racemosa. Conserv Biol 11:361–366

    Article  Google Scholar 

  • Guo D, Zhang H, Luo Z (2006) Genetic relationships of Diospyros kaki Thunb. and related species revealed by IRAP and REMAP analysis. Plant Sci 170:528–533

  • Hoebee SE, Young AG (2001) Low neighbourhood size and high interpopulation differentiation in the endangered shrub Grevillea iaspicula Mc Gill (Proteaceae). Heredity 86:489–496

  • Holsinger KE, Gottlieb LD (1991) Conservation of rare and endangered plants: principles and prospects. In Falk DA, Holsinger KE (eds) Genetics and Conservation of Rare Plants. Oxford University Press, Oxford, pp 195–223

    Google Scholar 

  • Houlden BA, Costello BH, Sharkey D, Fowler EV, Melzer A, Ellis W, Carrick F, Baverstock PR, Elphinstone MS (1996) Phylogeographic differentiation in the mitochondrial contro region in the koala Phascolarctos cinereus (Goldfuss, 1817). Mol Ecol 8:999–1011

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2001) IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, UK. Iiii+30pp. Downloadable from http://www.iucnredlist.org/info/categories_criteria

  • Kalendar R, Grob T, Regina M, Suoniemi A, Schulman A (1999) IRAP and REMAP: two new retrotransposon-based fingerprinting techniques. Theor Appl Genet 98:704–711

    Article  CAS  Google Scholar 

  • Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1(5):2478–2484

    Article  CAS  PubMed  Google Scholar 

  • Kalpoutzakis, E, Constantinidis TH (2009) Minuartia parnonia. In Phitos D, Constantinidis TH, Kamari G. (eds) The Red Data Book of Rare and Threatened Plants of Greece. Hellenic Botanical Society, Patras, pp 189–191 (in Greek)

    Google Scholar 

  • Kargiolaki H, Thanos CA, Fournaraki C, Maria EA, Karpathaki H (2007) Plant Micro-Reserves (A Pilot Project Implemented In Western Crete & Samaria Biosphere Reserve) In Priorities for Conservation of Biodiversity in Biosphere Reserves in Changing Conditions, pp 17–23, Proceedings from the International Conference, MAB UNESCO, 2–6 June 2007, Stará Lesná, Slovakia

  • Kruckeberg AR (1986) An essay: the stimulus of unusual geologies for plant speciation. Syst Bot 11:455–463

    Article  Google Scholar 

  • Laguna E (2001) The micro-reserves as a tool for conservation of threatened plants in Europe. Nature and Environment, No 121, Council of Europe Publishing.

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

    Article  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  CAS  PubMed  Google Scholar 

  • Macnair MR, Gardner M (1998) The evolution of edaphic endemics. In: Howard DJ, Berlocher SH (eds) Endless Forms: Species and Speciation. Oxford University Press, New York, pp. 157–171

    Google Scholar 

  • Mandoulakani BA, Piri Y, Darvishzadeh R, Bernoosi I, Jafari M (2012) Retroelement Insertional Polymorphism and Genetic Diversity in Medicago sativa Populations Revealed by IRAP and REMAP Markers. Plant Mol Biol Rep 30:286–296

    Article  Google Scholar 

  • McNeill J (1962) Taxonomic studies in the Alsinoideae II. A revision of the species in the Orient. Notes Roy Bot Gard Edinburgh 24:241–426

    Google Scholar 

  • Mengoni A, Barabesi C, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2001) Genetic diversity of heavy metal-tolerant populations in Silene paradoxa L. (Caryophyllaceae): a chloroplast microsatellite analysis. Mol Ecol 10:1909–1916

    Article  CAS  PubMed  Google Scholar 

  • Meulenkamp JE (1985) Aspects of the Late Cenozoic evolution of the Aegean region. In Stanley DJ, Wezel FC (eds) Geological evolution of the Mediterranean basin. Springer-Verlag, New York, pp 307–321

    Chapter  Google Scholar 

  • Miller MP (1997) Tools for Population Genetic Analysis (TFPGA), 1.3: A Windows Program for the Analysis of Allozyme and Molecular Population Genetic Data. Distributed by the author.

  • Mondini L, Noorani A, Pagnotta MA (2009) Assessing Plant Genetic Diversity using Molecular Tools. Diversity 1(1):19–35

    Article  CAS  Google Scholar 

  • Moore AJ, Merges D, Kadereit JW (2013) The origin of the serpentine endemic Minuartia laricifolia subsp. ophiolitica by vicariance and competitive exclusion. Mol Ecol 22:2218–2231

    Article  CAS  PubMed  Google Scholar 

  • Moore AJ, Kadereit JW (2013) The evolution of substrate differentiation in Minuartia series Laricifoliae (Caryophyllaceae) in the European Alps: in situ origin or repeated colonization? Am J Bot 100:2412–2425

    Article  PubMed  Google Scholar 

  • Nicoletti F, De Benedetti L, Airò M, Ruffoni B, Mercuri A, Minuto L, Casazza G (2012) Spatial genetic structure of Campanula sabatia, a threatened narrow endemic species of the Mediterranean Basin. Folia Geobot 47:249–262

    Article  Google Scholar 

  • Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357

    CAS  PubMed  Google Scholar 

  • Pandotra P, Husain MK, Ram R, Gupta S, Gupta AP (2013) Retrotransposon based genetic status of North-West Himalayan Zingiber officinale revealed high heterogeneity. J Plant Biochem Biot DOI 10.1007/s13562‒013‒0196‒8

    Google Scholar 

  • Paschke M, Abstract C, Schmid B (2002) Relationship between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica. Conserv Genet 3:131–144.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Phitos D, Constantinidis TH, Kamari G (eds) 2009. The Red Data Book of Rare and Threatened Plants of Greece, Vol. 2 (E-Z). Patras

  • Prentice HC, Malm JU, Mateu-Andrιs I, Segarra-Moragues JG (2003) Allozyme and chloroplast DNA variation in island and mainland populations of the rare Spanish endemic, Silene hifacensis (Caryophyllaceae). Conserv Genet 4:543–555

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Provan J, Biss MA, McMeel D, Mathews SH (2004) Universal primers for the amplification of chloroplast microsatellites in grasses (Poaceae). Mol Ecol Notes 4:262–264

    Article  CAS  Google Scholar 

  • Quintela-Sabarís C, Vendramin GG, Castro-Fernández D, Fraga MI (2010) Chloroplast microsatellites reveal that metallicolous populations of the Mediterranean shrub Cistus ladanifer L. have multiple origins. Plant Soil 334:161–174

    Article  Google Scholar 

  • Segarra-Moragues JG, Palop-Esteban A, Gonzales-Candelas F, Catalan P (2005) On the verge of extinction: genetics of the critically endangered Iberian plant species, Borderea chouardii (Dioscoreaceae) and implications for conservation management. Mol Ecol 14:969–982

    Article  CAS  PubMed  Google Scholar 

  • Setoguchi H, Mitsui Y, Ikeda H, Nomura N, Tamura A (2011) Genetic structure of the critically endangered plant Tricyrtis ishiiana (Convallariaceae) in relict populations of Japan. Conserv Genet 12:491–501

    Article  Google Scholar 

  • Shimono Y, Watanabe M, Hirao AS, Wada N, Kudo G (2009) Morphological and genetic variations of Potentilla matsumurae (Rosaceae) between fellfield and snowbed populations. Am J Bot 96:728–737

    Article  PubMed  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  CAS  PubMed  Google Scholar 

  • StatSoft Inc. (2004) STATISTICA (Data Analysis Software System), version 7

  • Till-Bottraud I, Gaudeul M (2002) Intraspecific genetic diversity in alpine plants. In Körner C, Spehn EM (eds), Mountain Biodiversity: A Global Assessment.Parthenon Publishing, New York, pp 23–34

    Google Scholar 

  • Trigas P, Iatrou G (2005) A new species of Minuartia (Caryophyllaceae) from the island of Evvia (Greece). Nordic J Bot 23:415–425

    Article  Google Scholar 

  • Trigas P, Iatrou G, Karetsos G (2007) Species diversity, endemism and conservation of the family Caryophyllaceae in Greece. Biodivers Conserv 16:357–376

    Article  Google Scholar 

  • Trigas P, Smyrni V (2009) Minuartia dirphya. In: Phitos D, Constantinidis TH, Kamari G (eds) The Red Data Book of Rare and Threatened Plants of Greece. Hellenic Botanical Society, Patras, pp. 186–188 (in Greek)

    Google Scholar 

  • Turland N, Kamari G (2009) Minuartia wettsteinii. In Phitos D, Constantinidis TH, Kamari G (eds) The Red Data Book of Rare and Threatened Plants of Greece. Hellenic Botanical Society, Patras, pp. 186–188 (in Greek)

    Google Scholar 

  • Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  CAS  PubMed  Google Scholar 

  • Weising K, Gardner R (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphism in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    Article  CAS  PubMed  Google Scholar 

  • Wise CA, Ranker TA, Linhart YB (2002) Modeling problems in conservation genetics with Brassica rapa. I. Genetic variation and fitness in plants under mild, stable conditions. Conserv Biol 16:1542–1554

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang J, Yang J, Yang M, Qing H (2012) Genetic diversity of Caragana species of the Ordos Plateau in China. Plant Syst Evol 298:801–809

    Article  Google Scholar 

  • Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, the User-Friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada

    Google Scholar 

  • Zheng L (1997) Microsatellite mapping of insect genomes. In Crampton JM, Beard CB, Louis C (eds) Molecular Biology of Insect Disease Vectors: A methods manual. Chapman & Hall, London, pp 309–320

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr E. Dionyssopoulou for her technical assistance, Professors A. Zacharopoulou and G. Kilias at the Department of Biology, University of Patras, Greece, for their generous support throughout this study and the two anonymous reviewers for their valuable comments. The authors also wish to declare that the experiments performed in this study comply with the current laws of Greece.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vassilis Papasotiropoulos.

Additional information

A. Augustinos and K. Sotirakis: co-first authors

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Augustinos, A., Sotirakis, K., Trigas, P. et al. Genetic Variation in Three Closely Related Minuartia (Caryophyllaceae) Species Endemic to Greece: Implications for Conservation Management. Folia Geobot 49, 603–621 (2014). https://doi.org/10.1007/s12224-014-9196-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12224-014-9196-2

Keywords

Navigation