Small genomes dominate in plants growing on serpentine soils in West Balkans, an exhaustive study of 8 habitats covering 308 taxa

Abstract

Aims

Habitats on ultramafic substrate present a hostile environment for plant development. We aimed to determine whether any particular range of genome size is favoured in such habitats.

Methods

Genome sizes of natural serpentinophyte populations were estimated using propidium iodide cytometry and compared with published data by phylogeny paired t-tests with plants from other substrata.

Results

The panel included 308 taxa belonging to 213 genera, with new values for 28 genera and 93 species. Using Leitch’s criteria, 56 % taxa belong to the group very small genomes (1C ≤ 1.4 pg), 22 % to small (1.4–3.5 pg), 19 % to intermediary (3.5–14 pg), 3 % to large (14–35 pg) and 0.31 % to very large (1C ≥ 35 pg). The majority of species were either indifferent for substrate (56 %) or facultative serpentinophytes (33 %). Most obligate serpentinophytes possessed very small genomes, and none exceeded 5 pg (1C). On average, plants growing on serpentine exhibited lower Cx-values than the same taxa growing on other soil types. About 4 % of species were annuals and 88 % perennials. Hemicryptophytes were dominant. Presence of at least two ploidy levels was recorded for 10 species.

Conclusions

Water stress, high temperatures and presence of heavy metals in serpentine habitats impose a high selective pressure and favour perennial species with very small genomes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

2C DNA:

DNA content of one replicated holoploid genome

1C DNA:

DNA content of one non-replicated holoploid genome

1Cx-value:

Monoploid genome size

pg:

Picogramme

Mbp:

Mega base pair

References

  1. APG (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Article  Google Scholar 

  2. Baker AJM, Proctor J, Reeves RD (1992) The vegetation of ultramafic (serpentine) soils. Proceedings of the First International Conference on Serpentine Ecology, University of California, Davis, 19–22 June 1991. Intercept, Hampshire, UK. pp 509

  3. Bancheva S, Greilhuber J (2006) Genome size in Bulgarian Centaurea s.l. (Asteraceae). Plant Syst Evol 257:95–117

    Article  CAS  Google Scholar 

  4. Bennett MD (1972) Nuclear DNA content and minimum generation time in herbaceous plants. Proc R Soc Lond B 181:109–135

    PubMed  Article  CAS  Google Scholar 

  5. Bennett MD (1987) Variation in genomic form in plants and its ecological implications. New Phytol 106(Suppl):177–200

    Google Scholar 

  6. Bennett MD, Leitch IJ (2010) Angiosperm DNA C-values database (release 5.0), Royal Botanic Gardens, Kew. http://www.rbgkew.org.uk/cval/homepage.html

  7. Bennett MD, Smith JB, Lewis Smith RI (1982) DNA amounts of angiosperms from the Antarctic and South Georgia. Environ Exp Bot 22:307–318

    Article  Google Scholar 

  8. Bennett MD, Leitch IJ, Hanson L (1998) DNA amounts in two samples of angiosperm weeds. Ann Bot 82(Suppl A):121–134

    Article  Google Scholar 

  9. Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132

    PubMed  Article  CAS  Google Scholar 

  10. Blondon F, Marie D, Brown SC, Kondorosi A (1994) Genome size and base composition in Medicago sativa and M. Truncatula species. Genome 37:264–270

    PubMed  Article  CAS  Google Scholar 

  11. Bogunic F, Muratovic E, Brown S, Siljak-Yakovlev S (2003) Genome size and base composition of five Pinus species from Balkan region. Plant Cell Rep 22:59–63

    PubMed  Article  CAS  Google Scholar 

  12. Bogunic F, Muratovic E, Ballian D, Siljak-Yakovlev S, Brown S (2007) Genome size stability among five subspecies of Pinus nigra Arnold s.l. Environ Exp Bot 59:345–360

    Article  Google Scholar 

  13. Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol S 36:243–266

    Article  Google Scholar 

  14. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Oregon

    Google Scholar 

  15. Cerbah M, Coulaud J, Brown SC, Siljak-Yakovlev S (1999) Evolutionary DNA variation in the genus Hypochaeris. Heredity 82:261–266

    PubMed  Article  CAS  Google Scholar 

  16. Cerbah M, Montreau E, Brown S, Siljak-Yakovlev S, Bertrand H, Lambert C (2001) Genome size variation and species relationships in the genus Hydrangea. Theor Appl Genet 103:45–51

    Article  CAS  Google Scholar 

  17. Chiarucci A (2004) Vegetation ecology and conservation on Tuscan ultramafic soils. Bot Rev 69:252–268

    Article  Google Scholar 

  18. Chiarucci A, Roccihini D, Leonzio C, De Dominicis V (2001) A test of vegetation-environment relationship in serpentine soils of Tuscany, Italy. Ecol Res 16:627–639

    Article  Google Scholar 

  19. Chiarucci A, Bonini I, Fattorini L (2003) Community dynamics of serpentine vegetation in relation to nutrient addition and climatic variability. J Mediterr Ecol 4:23–30

    Google Scholar 

  20. Coba de la Peña T, Brown SC (2001) Cytometry and fluorimetry. In: Hawes C, Satiat-Jeunemaître B (eds) Plant cell biology: a practical approach. Oxford University Press, Oxford, pp 85–106

    Google Scholar 

  21. Coleman RG, Jove C (1992) Geological origin of serpentinites. In: Baker AJM, Proctor J, Reeves RD (eds) The Vegetation of Ultramafic (Serpentine) Soils. Intercept, Andover, pp 1–18

  22. Cuénoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ, Chase MW (2002) Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. Am J Bot 89:132–144

    PubMed  Article  Google Scholar 

  23. Darlington CD, Wylie A (1955) Chromosome atlas of flowering plants. George Allen and Unwin, London

    Google Scholar 

  24. Dimitrova D, Greilhuber J (2000) Karyotype and DNA-content evolution in ten species of Crepis (Asteraceae) distributed in Bulgaria. Bot J Linn Soc 132:281–297

    Article  Google Scholar 

  25. Dolezel J, Bartos J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry 51:127–128

    PubMed  Article  CAS  Google Scholar 

  26. Doležel J, Greilhuber J, Suda J (2007) Flow cytometry with plant cells. Wiley-VCH Verlag, Weinheim

    Book  Google Scholar 

  27. Fedorov AA (1969) Chromosome numbers of flowering plants. Academy of sciences of the USSR, V. L. Komarov Botanical Institute, Nauka, Leningrad

    Google Scholar 

  28. Galbraith D, Harkins K, Maddoks J, Ayres N, Sharma D, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051

    PubMed  Article  CAS  Google Scholar 

  29. Garnatje T, Valles J, Garcia S, Hidalgo O, Sanz M, Canela MA, Siljak-Yakovlev S (2004) Genome size in Echinops L. and related genera (Asteraceae, Cardueae): karyological, ecological and phylogenetic implications. Biol Cell 96:117–124

    PubMed  Article  CAS  Google Scholar 

  30. Godelle B, Cartier D, Marie D, Brown SC, Siljak-Yakovlev S (1993) Heterochromatin study demonstrating the non-linearity of fluorometry useful for calculating genomic base composition. Cytometry 14:618–626

    PubMed  Article  CAS  Google Scholar 

  31. Goldblatt P (1981) Index to Plant Chromosome Numbers 1975–1978. Monographs in Systematic Botany from the Missouri Botanical Garden, v. 5. Saint Louis: Missouri Botanical Garden

  32. Goldblatt P, Johnson DE (2006) Index to Plant Chromosome Numbers 2001–2003. Monographs in systematic botany from the Missouri Botanical Garden 106, St. Louis. http://www.tropicos.org/Project/IPCN

  33. Grafen A (1989) The phylogenetic regression. Phil Trans R Soc Lond B Biol Sci 326:119–157

    Article  CAS  Google Scholar 

  34. Gregory TR (2001) Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev 76:65–101

    PubMed  Article  CAS  Google Scholar 

  35. Greilhuber J, Doležel J, Lysak MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms “genome size” and “C-value” to describe nuclear DNA contents. Ann Bot 95:255–260

    PubMed  Article  CAS  Google Scholar 

  36. Grime JP, Mowforth MA (1982) Variation in genome size – an ecological interpretation. Nature 299:151–153

    Article  Google Scholar 

  37. Hajrudinović A (2012) Veličina genoma i morfološki diverzitet vrsta Sorbus aria i S. austriaca određenih bosanskohercegovačkih populacija. MSc Thesis, University of Sarajevo, Bosnia and Herzegovina (in Bosnian)

  38. Harrison S, Safford HD, Grace JB, Viers JH, Davies KF (2006) Regional and local species richness in an insular environment: serpentine plants in California. Ecol Monogr 76:41–56

    Article  Google Scholar 

  39. Hodgson JG, Sharafi M, Jalili A, Díaz S, Montserrat-Martí G, Palmer C, Cerabolini B, Pierce S, Hamzehee B, Asri Y, Jamzad Z, Wilson P, Raven JA, Band SR, Basconcelo S, Bogard A, Carter G, Charles M, Castro-Díez P, Cornelissen JHC, Funes G, Jones G, Khoshnevis M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Boustani S, Dehghan M, Guerrero-Campo J, Hynd A, Kowsary E, Kazemi-Saeed F, Siavash B, Villar-Salvador P, Craigie R, Naqinezhad A, Romo-Díez A, de Torres EL, Simmons E (2010) Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Ann Bot 105:573–584

    PubMed  Article  CAS  Google Scholar 

  40. Jakob SS, Meister A, Blattner FR (2004) Considerable genome size variation of Hordeum species (Poaceae) is linked to phylogeny, life form, ecology, and speciation rates. Mol Biol Evol 21:860–869

    PubMed  Article  CAS  Google Scholar 

  41. Jenny H (1980) The soil resource: Origin and behaviour. Ecological studies 37. Springer, New York

    Google Scholar 

  42. Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    PubMed  CAS  Google Scholar 

  43. Knight CA, Ackerly DD (2002) Variation in nuclear DNA content across environmental gradients: a quantile regression analysis. Ecol Lett 5:66–76

    Article  Google Scholar 

  44. Knight CA, Beaulieu JM (2008) Genome size scaling through phenotype space. Ann Bot 101:759–766

    PubMed  Article  Google Scholar 

  45. Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 95:177–190

    PubMed  Article  CAS  Google Scholar 

  46. Kolář F, Fér T, Štech M, Trávníček P, Dušková E, Schönswetter P, Suda J (2012) Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae). PLoS One 7:e39988. doi:10.1371/journal.pone.0039988

    PubMed  Article  Google Scholar 

  47. Kruckeberg AR (1984) California serpentines: flora, vegetation, geology, soils and management problems. University of California Press, Berkeley

    Google Scholar 

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

    Article  Google Scholar 

  49. Kruckeberg AR (2002) Geology and plant life: the effects of landforms and rock types on plants, 1st edn. University Washington Press, Seattle/London

    Google Scholar 

  50. Kubeševá M, Moravcová L, Suda J, Jarošík V, Pyšek P (2010) Naturalized plants have smaller genomes than their non-invading relatives: a flow cytometric analysis of the Czech alien flora. Preslia 82:81–96

    Google Scholar 

  51. Le Thierry d’Ennequin M, Panaud O, Siljak-Yakovlev S, Sarr A (1998) First evaluation of nuclear DNA content in Setaria genus by flow cytometry. J Hered 89:556–559

    Article  Google Scholar 

  52. Leitch IJ, Bennett MD (2007) Genome size and its uses: the impact of flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells. Wiley-VCH Verlag, Weinheim, pp 153–176

    Google Scholar 

  53. Leitch IJ, Chase MW, Bennett MD (1998) Phylogenetic analysis of DNA C-values provides evidence for a small ancestral genome size in flowering plants. Ann Bot 82(suppl A):85–94

    Google Scholar 

  54. Lepers-Andrzejewski S, Siljak-Yakovlev S, Brown SC, Wong M, Dron M (2011) Diversity and dynamics of plant genome size: an example of polysomaty from a cytogenetic study of Tahitian Vanilla (Vanilla xtahitensis, Orchidaceae). Am J Bot 98:986–997

    PubMed  Article  Google Scholar 

  55. Li R-Q, Chen Z-D, Lu A-M, Soltis DE, Soltis PS, Manos PS (2004) Phylogenetic relationships in Fagales based on DNA sequences from three genomes. Int J Plant Sci 165:311–324

    Article  CAS  Google Scholar 

  56. Lindenfors P, Revell LJ, Nunn CL (2010) Sexual dimorphism in primate aerobic capacity: a phylogenetic test. J Evol Biol 23:1183–1194

    PubMed  Article  Google Scholar 

  57. Loureiro J, Rodriguez E, Santos C, Doležel J, Suda J (2008) FLOWer: a plant DNA flow cytometry database (release 1.0, May 2008), http://flower.web.ua.pt/

  58. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    PubMed  Article  CAS  Google Scholar 

  59. Marie D, Brown SC (1993) A cytometric exercise in plant DNA histograms with 2C values for 70 species. Biol Cell 78:41–51

    PubMed  Article  CAS  Google Scholar 

  60. Martel E, De Nay D, Siljak-Yakovlev S, Brown S, Sarr A (1997) Genome size variation and basic chromosome number in pearl millet and fourteen related Pennisetum species. J Hered 88:139–143

    Article  Google Scholar 

  61. Mueller-Dombois D, Ellenberg H (1974) Aims and methods of vegetation ecology, 1st edn. John Wiley & Sons Inc., New York

    Google Scholar 

  62. Muratović E, Hidalgo O, Garnatje T, Siljak-Yakovlev S (2010) Molecular phylogeny and genome size in European lilies (Genus Lilium, Liliaceae). Adv Sci Lett 3:180–189

    Article  Google Scholar 

  63. Oberprieler C, Himmelreich S, Vogt R (2007) A new subtribal classification of the tribe Anthemideae (Compositae). Willdenowia 37:89–114

    Article  Google Scholar 

  64. Ohri D (1998) Genome size variation and plant systematic. Ann Bot 82:75–83

    Article  Google Scholar 

  65. Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM (2007) The mode and tempo of genome size evolution in eukaryotes. Genome Res 17:594–601

    PubMed  Article  CAS  Google Scholar 

  66. Pavlova DK (2010) A survey of the serpentine flora in the West Bulgarian Frontier Mts (Mt Vlahina and Mt Ograzhden). Phytol Balc 16:97–107

    Google Scholar 

  67. Pellicer J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linn Soc 164:10–15

    Article  Google Scholar 

  68. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of rosaceae. Plant Syst Evol 266:5–43

    Article  Google Scholar 

  69. Preston JC, Martinez CC, Hileman LC (2011) Gradual desintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome. PNAS USA 108:2343–2348

    PubMed  Article  CAS  Google Scholar 

  70. Price HJ, Johnston JS (1996) Analysis of plant DNA content by Feulgen micro-spectrophotometry and flow cytometry. In: Jauhur P (ed) Methods of genome analysis in plants: their merits and pitfalls. CRC Press, Boca Raton, pp 115–132

    Google Scholar 

  71. Proctor J (1999) Toxins, nutrient shortages and droughts: the serpentine challenge. Tree 14:334–335

    Google Scholar 

  72. Proctor J, Nagy L (1992) Ultramafic rocks and their vegetation: an overview. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd, Andover, pp 469–494

    Google Scholar 

  73. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, www.R-project.org

  74. Rajakaruna N, Baker AJM (2004) Serpentine: a model habitat for botanical research in Sri Lanka. Ceylon J Sci (Biol Sci) 32:1–19

    Google Scholar 

  75. Rajakaruna N, Bohm BA (2002) Serpentine and its vegetation: a preliminary study from Sri Lanka. J Appl Bot 76:20–28

    Google Scholar 

  76. Rajakaruna N, Whitton J (2004) Trends in the evolution of edaphic specialists with an example of parallel evolution in the Lasthenia californica complex. In: Cronk QCB, Taylor IEP, Ree R, Whitton J (eds) Plant adaptation: Molecular Biology and Ecology. NRC Canada Reasearch Press Vancouver, University of British Columbia, pp 103–110

  77. Riter-Studnička H (1963) Biljni pokrov na serpentinima u Bosni. God Biol Ins Univ Sarajevo 14:91–204 (in Bosnian)

    Google Scholar 

  78. Riter-Studnička H (1964) Anatomske razlike između biljaka sa serpentinske, dolomitne i krečnjačke podloge. God Biol Inst Univ Sarajevo 17:161–197 (in Bosnian)

    Google Scholar 

  79. Roberts BA, Proctor J (1992) The ecology of areas with serpentinized rocks. A world view. Kluwer Academic Publications, Dordrecht

    Book  Google Scholar 

  80. Schäferhoff B, Fleischmann A, Fischer E, Albach DC, Borsch T, Heubl G, Müller KF (2010) Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evo Biol 10:352

    Article  Google Scholar 

  81. Selvi F (2007) Diversity, geographic variation and conservation of the serpentine flora of Tuscany (Italy). Biodivers Conserv 16:1423–1439

    Article  Google Scholar 

  82. Siljak-Yakovlev S, Cerbah M, Coulaud J, Stoian V, Brown SC, Jelenic S, Papeš D (2002) Nuclear DNA content, base composition, heterochromatin and rDNA in Picea omorika and Picea abies. Theor Appl Genet 104:505–512

    PubMed  Article  CAS  Google Scholar 

  83. Siljak-Yakovlev S, Solic EM, Catrice O, Brown SC, Papes D (2005) Genome size and chromosome number in some Centaurea (Asteraceae: Cardueae) from Dalmatia region. Plant Biol 7:397–404

    PubMed  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  85. Siljak-Yakovlev S, Pustahija F, Šolić EM, Bogunić F, Muratović E, Bašić N, Catrice O, Brown SC (2010) Towards a genome size and chromosome number database of Balkan flora: C-values in 343 taxa with novel values for 242. Adv Sci Lett 3:190–224

    Article  CAS  Google Scholar 

  86. Slovák M, Vit P, Urfus T, Suda J (2009) Complex pattern of genome size variation in a polymorphic member of the Asteraceae. J Biogeogr 36:372–384

    Article  Google Scholar 

  87. Stevanović V, Tan K, Iatrou G (2003) Distribution of the endemic Balkan flora on serpentine I. – obligate serpentine endemics. Plant Syst Evol 242:149–170

    Article  Google Scholar 

  88. Talent N, Dickinson TA (2005) Polyploidy in Crataegus and Mespilus (Rosaceae, Maloideae): evolutionary inferences from flow cytometry of nuclear DNA amounts. Can J Bot 83:1268–1304

    Article  CAS  Google Scholar 

  89. te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? the role of polyploidy in facilitating plant invasions. Ann Bot. doi:10.1093/aob/mcr277

    Google Scholar 

  90. Temsch EM, Temsch W, Ehrendorfer-Schratt L, Greilhuber J (2010) Heavy metal pollution, selection, and genome size: the species of the Žerjav study revisited with flow cytometry. J Bot. doi:10.1155/2010/596542

    Google Scholar 

  91. Torices R (2010) Adding time-calibrated branch lengths to the Asteraceae supertree. J Syst Evol 48:271–278

    Article  Google Scholar 

  92. Torrel M, Vallès J (2001) Genome size in 21 Artemisia L. species (Asteraceae, Anthemideae): systematic, evolutionary, and ecologicaly implications. Genome 44:231–238

    Google Scholar 

  93. Vekemans X, Lefebvre C, Coulaud J, Blaise S, Gruber W, Siljak-Yakovlev S, Brown SC (1996) Variation in nuclear DNA content at the species level in Armeria maritima. Hereditas 124:237–242

    Article  Google Scholar 

  94. Veselý P, Bureš P, Šmarda P, Pavlíček T (2012) Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Ann Bot 109:65–75

    PubMed  Article  Google Scholar 

  95. Vidic T, Greilhuber J, Vilhar B, Dermastia M (2009) Selective significance of genome size in a plant community with heavy metal pollution. Ecol Appl 19:1515–1521

    PubMed  Article  CAS  Google Scholar 

  96. Vinogradov AE (2003) Selfish DNA is maladaptive: evidence from the plant Red List. Trends Genet 19:609–614

    PubMed  Article  CAS  Google Scholar 

  97. Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242

    PubMed  Article  Google Scholar 

  98. Wang X-Q, Tank DC, Sang T (2000) Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17:773–781

    PubMed  Article  CAS  Google Scholar 

  99. Wang W, Lu A-M, Ren Y, Endress ME, Chen Z-D (2009) Phylogeny and classification of Ranunculales: evidences from four molecular loci and morphological data. Perspect Plant Ecol Evol Syst 11:81–110

    Article  Google Scholar 

  100. Whitney KD, Garland T Jr (2010) Did genetic drift drive increases in genome complexity? PLoS Genetics 6:e1001080

    PubMed  Article  Google Scholar 

  101. Whitney KD, Baack EJ, Hamrick JL, Godt MJW, Barringer BC, Bennett MD, Eckert CG, Goodwillie C, Kalisz S, Leitch IJ, Ross-Ibarra J (2010) A role for nonadaptive processes in plant genome size evolution? Evol 64:2097–2109

    Google Scholar 

  102. Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Amer J Bot 91:1846–1862

    Article  CAS  Google Scholar 

  103. Zhang J-W, Nie Z-L, Wen J, Sun H (2011) Moleculr phylogeny and biogeography of three closely related genera, Soroseris, Stebbinsia, and Syncalathium (Asteraceae, Cichorieae), endemic to the Tibetan Plateau, SW China. Taxon 60:15–26

  104. Zonneveld BJM (2008) The systematic value of nuclear DNA content for all species of Narcissus L. (Amaryllidaceae). Plant Syst Evol 275:109–132

    Article  CAS  Google Scholar 

  105. Zonneveld BJM, Leitch IJ, Bennett MD (2005) First nuclear DNA amounts in more than 300 Angiosperms. Ann Bot 96:229–244

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Nicolas Maunoury and Olivier Catrice for their assistance on the IBiSA Cytometry Platform of the Imagif Cell Biology Unit of the Gif campus (www.imagif.cnrs.fr). We also thank the IFR87 La plante et son environnement, and the anonymous reviewers for their valuable comments to improve the quality of the paper. This study was financially supported by the Regional grant Ile de France (SETCI R232) for a co-tutelle PhD and NATO “Science For Peace and Security” Programme (Collaborative Linkage Grant). O. H. benefitted from a ‘Juan de la Cierva’ contract (JCI-2010- 07516). V. Stevanović was supported by Ministry of Education, Science and Technology of Serbia (Grant no. 173030).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Fatima Pustahija.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Suppl. Fig. S1
figure9

Cumulative frequency curves of 1C genome size for three increasingly harsh environments: A) 103 taxa from calcareous littoral communities (Mt Biokovo, Croatia; Siljak-Yakovlev et al. 2010); B) 68 taxa from several continental calcareous mountains (Central Bosnia, Bosnia and Herzegovina, Siljak-Yakovlev et al. 2010) and C) 308 serpentine taxa (present study). The median values (arrows) are indicated for each curve: 1.55, 1.37 and 1.25 pg respectively. (JPEG 90.5 kb)

Table S1

Comparison of our data and 332 published 1C-values (pg), chromosome number (2n) and ploidy level (x) concerning 210 taxa. (DOC 606 kb)

Table S2

List of the 83 taxa used to carry out the phylogenetic t-test, indicating for each taxa the 1Cx-value (pg) on serpentines, the 1Cx-value (pg) on other substrate and the ploidy level (x). (DOC 156 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pustahija, F., Brown, S.C., Bogunić, F. et al. Small genomes dominate in plants growing on serpentine soils in West Balkans, an exhaustive study of 8 habitats covering 308 taxa. Plant Soil 373, 427–453 (2013). https://doi.org/10.1007/s11104-013-1794-x

Download citation

Keywords

  • 2C DNA
  • Chromosome number
  • Phylogenetic paired t-test
  • Ploidy
  • Serpentinophytes
  • Ultramafic substrate