BACKGROUND AND AIMS: Although the large variation in genome size among different species is widely acknowledged, the occurrence and extent of variation below the species level are still controversial and have not yet been satisfactorily analysed. The aim of this study was to assess genome size variation in six ploidy levels (2n = 3x-8x) of the polyploid Allium oleraceum over a large geographical gradient and to search for potential interpretations of the size variation. METHODS: The genome sizes of 407 individuals of A. oleraceum collected from 114 populations across Europe were determined by flow cytometry using propidium iodide staining. The genome size variation was correlated with spatial, climatic and habitat variables. KEY RESULTS: The mean holoploid genome size (2C DNA) was 42·49, 52·14, 63·34, 71·94, 85·51 and 92·12 pg at the tri-, tetra-, penta-, hexa-, hepta- and octoploid levels, respectively. Genome size varied from a minimum of 2·3 % in the octoploids to a maximum of 18·3 % in the tetraploids. Spatial structuring of genome size was observed within the tetra- and pentaploids, where 2C DNA significantly increased with both latitude and longitude, and correlated with several climatic variables, suggesting a gradient of continentality. Genome size in hexaploids showed low variation, weak correlation with climatic variables and no spatial structuring. Downsizing in monoploid genome size was observed between all cytotypes except for heptaploids. Splitting populations into western and eastern European groups resulted in strong differences in monoploid genome size between groups in tetra- and pentaploids but not in hexaploids. The monoploid genome sizes of the cytotypes were similar in the western group but diverged in the eastern group. CONCLUSIONS: Complex patterns of holoploid and monoploid genome size variation found both within and between A. oleraceum cytotypes are most likely the result of several interacting factors, including different evolutionary origins of cytotypes via hybridization of parental combinations with different genome sizes in the south-western and south-eastern part of Europe, introgression between cytotypes, and antropic dispersal. The role of broad-scale and fine-scale environmental variables in shaping genome size is probably of minor importance in A. oleraceum.

Plant Biosystematics and Ecology Research Group Department of Botany Faculty of Science Palacký University Šlechtitelů 11 CZ 783 71 Olomouc Czech Republic

Zobrazit více v PubMed

Balao F, Casimiro-Soriguer R, Talavera M, Herrera J, Talavera S. Distribution and diversity of cytotypes in Dianthus broteri as evidenced by genome size variations. Annals of Botany. 2009;104:965–973. PubMed PMC

Bancheva S, Greilhuber J. Genome size in Bulgarian Centaurea s.l. (Asteraceae) Plant Systematics and Evolution. 2006;257:95–117.

Baranyi M, Greilhuber J. Genome size in Allium: in quest of reproducible data. Annals of Botany. 1999;83:687–695.

Beaulieu JM, Leitch IJ, Knight CA. Genome size evolution in relation to leaf strategy and metabolic rates revisited. Annals of Botany. 2007a;99:495–505. PubMed PMC

Beaulieu JM, Moles AT, Leitch IJ, Bennett MD, Dickie JB, Knight CA. Correlated evolution of genome size and seed mass. New Phytologist. 2007b;173:422–437. PubMed

Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist. 2008;179:975–986. PubMed

te Beest M, Le Roux JJ, Richardson DM, et al. The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany. 2012;109:19–45. PubMed PMC

Bennett MD. Nuclear DNA content and minimum generation time in herbaceous plants. Proceedings of the Royal Society of London Series B. 1972;181:109–135. PubMed

Bennett MD. Variation in genomic form in plants and its ecological implications. New Phytologist. 1987;106:177–200.

Bennett MD, Leitch IJ. Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Annals of Botany. 2011;107:467–590. PubMed PMC

Bennetzen JL, Ma J, Devos KM. Mechanisms of recent genome size variation in flowering plants. Annals of Botany. 2005;95:127–132. PubMed PMC

Benor S, Fuchs J, Blattner FR. Genome size variation in Corchorus olitorius (Malvaceae s.l.) and its correlation with elevation and phenotypic traits. Genome. 2011;54:575–585. PubMed

Benson NA, Braylan RC. Evaluation of sensitivity in DNA aneuploidy detection using a mathematical model. Cytometry. 1994;15:53–58. PubMed

Biémont C. Within-species variation in genome size. Heredity. 2008;101:297–298. PubMed

Bogdanovič S, Brullo S, del Galdo GG, Salmeri C. A new autumn-flowering species of Allium (Alliaceae) from Croatia. Folia Geobotanica. 2009;44:83–93.

Brullo S, Pavone P, Salmeri C. Cytotaxonomical notes on Allium dentiferum Webb & Bethelot, an unknown species of the Mediterranean flora. Botanica Chronika. 1991;10:785–796.

Burešová V. Comparative morphology of cytotypes of Allium oleraceum. Olomouc, Czech Republic: Department of Botany, Palacký University; 2012. MSc thesis.

Cavalier-Smith T. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Annals of Botany. 2005;95:147–175. PubMed PMC

Ceccarelli M, Sarri V, Caceres ME, Cionini PG. Intraspecific genotypic diversity in plants. Genome. 2011;54:701–709. PubMed

Chen ZJ. Molecular mechanisms of polyploidy and hybrid vigor. Trends in Plant Science. 2010;15:57–71. PubMed PMC

Chrtek J, Zahradníček J, Krak K, Fehrer J. Genome size in Hieracium subgenus Hieracium (Asteraceae) is strongly correlated with major phylogenetic groups. Annals of Botany. 2009;104:161–178. PubMed PMC

Cires E, Cuesta C, Revilla MA, Prieto JAD. Intraspecific genome size variation and morphological differentiation of Ranunculus parnassifolius (Ranunculaceae), an Alpine–Pyrenean–Cantabrian polyploid group. Biological Journal of the Linnean Society. 2010;101:251–271.

Cosendai AC, Rodewald J, Hörandl E. Origin and evolution of apomixis via autopolyploidy in the alpine plant species Ranunculus kuepferi. Taxon. 2011;60:355–364.

Cressie NA. Statistics for spatial data. Revised edition. New York: Wiley; 1993.

Doležel J, Bartoš J. Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany. 2005;95:99–110. PubMed PMC

Doležel J, Greilhuber J, Lucretti S, et al. Plant genome size estimation by flow cytometry: inter-laboratory comparison. Annals of Botany. 1998;82(Suppl. A):17–26.

Doležel J, Greilhuber J, Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols. 2007;2:2233–2244. PubMed

Duchoslav M, Šafářová L, Krahulec F. Complex distribution patterns, ecology and coexistence of ploidy levels of Allium oleraceum (Alliaceae) in the Czech Republic. Annals of Botany. 2010;105:719–735. PubMed PMC

Ekrt L, Holubová R, Trávníček P, Suda J. Species boundaries and frequency of hybridization in the Dryopteris carthusiana (Dryopteridaceae) complex: a taxonomic puzzle resolved using genome size data. American Journal of Botany. 2010;97:1208–1219. PubMed

Fialová R. Polyploid complexes in the genus Allium. Olomouc, Czech Republic: Department of Botany, Faculty of Science, Palacký University; 1996. PhD thesis.

Francis D, Stuart-Davies M, Barlow PW. A strong nucleotypic effect on the cell cycle regardless of ploidy level. Annals of Botany. 2008;101:747–757. PubMed PMC

Friesen N. The genera Allium L. and Caloscordum Herbert. 1987. In: Malyshev L, Peshkova G, editors. Flora of Siberia: Araceae-Orchidaceae. Novosibirsk: Nauka, 177–195; 1987. (in Russian)

Friesen N, Fritsch R, Blattner F. Phylogeny and new intragenetic classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso. 2006;22:372–395.

Gregory TR. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biological Reviews. 2001;76:65–101. PubMed

Gregory TR. The C-value enigma in plants and animals: a review of parallels and an appeal for partnership. Annals of Botany. 2005;95:133–146. PubMed PMC

Greilhuber J. Intraspecific variation in genome size: a critical reassessment. Annals of Botany. 1998;82(Suppl. A):27–35.

Greilhuber J. Intraspecific variation in genome size in angiosperms: identifying its existence. Annals of Botany. 2005;95:91–98. PubMed PMC

Greilhuber J, Doležel J, Lysák MA, Bennett MD. The origin, evolution and proposed stabilization of the terms ‘Genome Size’ and ‘C-Value’ to describe nuclear DNA contents. Annals of Botany. 2005;95:255–260. PubMed PMC

Greilhuber J, Borsch T, Muller K, Worberg A, Porembski S, Barthlott W. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biology. 2006;8:770–777. PubMed

Greilhuber J, Temsch EM, Loureiro JCM. Nuclear DNA content measurement. In: Doležel J, Greilhuber J, Suda J, editors. Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Weinheim: Wiley; 2007. pp. 67–101.

Hewitt GM. Postglacial recolonization of European Biota. Biological Journal of the Linnean Society. 1999;68:87–112.

Hewitt GM. Genetic consequences of climatic oscillations in the quaternary. Philosophical Transactions of the Royal Society B: Biological Sciences. 2004;359:183–195. PubMed PMC

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology. 2005;25:1965–1978.

Hodgson JG, Sharafi M, Jalili A, et al. Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Annals of Botany. 2010;105:573–584. PubMed PMC

Jackson DA. Protest: a procrustean randomization test of community environment concordance. Ecoscience. 1995;2:297–303.

Jandová M. Cytogenetic study of generative offsprings in polyploid Allium oleraceum. Olomouc, Czech Republic: Department of Botany, Faculty of Science, Palacký University; 2010. MSc thesis.

Jírová A. Reproductive biology and phenology in polyploid Allium oleraceum. Olomouc, Czech Republic: Department of Botany, Faculty of Science, Palacký University; 2007. MSc thesis.

Karpavičienė B. Chromosome numbers of Allium from Lithuania. Annales Botanici Fennici. 2007;44:345–352.

Karpavičienė B. Morphological, reproductive and karyological variability in Allium oleraceum in Lithuania. Biologia. 2012;67:278–283.

Kim S, Rayburn AL, Parrish A, Lee DK. Cytogeographic distribution and genome size variation in prairie cordgrass (Spartina pectinata Bosc ex Link) Plant Molecular Biology Reporter. 2012;30:1073–1079.

Knight CA, Molinari NA, Petrov DA. The large genome constraint hypothesis: evolution, ecology and phenotype. Annals of Botany. 2005;95:177–190. PubMed PMC

Kubátová B, Trávníček P, Bastlová D, Čurn V, Jarolímová V, Suda J. DNA ploidy-level variation in native and invasive populations of Lythurum salicaria at a large geographical scale. Journal of Biogeography. 2008;35:167–176.

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

Labani RM, Elkington TT. Nuclear DNA variation in the genus Allium L. (Liliaceae) Heredity. 1987;59:119–128.

Lavergne S, Muenke NJ, Molofsky J. Genome size reduction can trigger rapid phenotypic evolution in invasive plants. Annals of Botany. 2010;105:109–116. PubMed PMC

Legendre P, Fortin MJ. Spatial patterns and ecological analysis. Vegetatio. 1989;80:107–138.

Legendre P, Legendre L. Numerical ecology. 2nd English edition. Amsterdam: Elsevier Science BV; 1998.

Leitch IJ, Bennett MD. Genome downsizing in polyploid plants. Biological Journal of the Linnean Society. 2004;82:651–663.

Levan A. Cytological studies in Allium paniculatum group. Hereditas. 1937;23:317–370.

Lichstein JW, Simons TR, Shriner SA, Franzreb KE. Spatial autocorrelation and autoregressive models in ecology. Ecological Monographs. 2002;72:445–463.

Loidl J. Some features of heterochromatin in wild Allium species. Plant Systematics and Evolution. 1983;143:117–131.

Loureiro J, Rodriguez E, Doležel J, Santos C. Flowcytometric and microscopic analysis of the effect of tannic acid on plant nuclei and estimation of DNA content. Annals of Botany. 2006;98:515–527. PubMed PMC

Loureiro J, Trávníček P, Rauchová J, et al. The use of flow cytometry in the biosystematics, ecology and population biology of homoploid plants. Preslia. 2010;82:3–21.

Lysák MA, Rostková A, Dixon JM, Rossi G, Doležel J. Limited genome size variation in Sesleria albicans. Annals of Botany. 2000;86:399–403.

Lysák MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ. The dynamic ups and downs of genome size evolution in Brassicaceae. Molecular Biology and Evolution. 2009;26(85–98) PubMed

MacGillivray CW, Grime JP. Genome size predicts frost resistance in British herbaceous plants: implications for rates of vegetation response to global warming. Functional Ecology. 1995;9:320–325.

Mahelka V, Suda J, Jarolímová V, Trávníček P, Krahulec F. Genome size discriminates between closely related taxa Elytrigia repens and E. intermedia (Poaceae: Triticeae) and their hybrid. Folia Geobotanica. 2005;40:367–384.

Meagher TR, Vassiliadis C. Phenotypic impacts of repetitive DNA in flowering plants. New Phytologist. 2005;168:71–80. PubMed

Meusel H, Jäger E, Weinert E. Vergleichende Chorologie der zentraleuropäischen Flora. Jena: Gustav Fischer Verlag; 1965.

Mráz P, Chrtek J, Šingliarová B. Geographical parthenogenesis, genome size variation and pollen production in the arctic–alpine species Hieracium alpinum. Botanica Helvetica. 2009;119:41–51.

Murray BG. When does intraspecific C-value variation become taxonomically significant? Annals of Botany. 2005;95:119–125. PubMed PMC

Ohri D. Climate and growth form: the consequences for genome size in plants. Plant Biology. 2005;7:449–458. PubMed

Ohri D, Fritsch RM, Hanelt P. Evolution of genome size in Allium (Alliaceae) Plant Systematics and Evolution. 1998;210:57–86.

Ohryzek J. Comparative biology of cytotypes of Allium oleraceum. Olomouc, Czech Republic: Department of Botany, Faculty of Science, Palacký University; 2007. MSc thesis.

Olšavská K, Perný M, Španiel S, Šingliarová B. Nuclear DNA content variation among perennial taxa of the genus Cyanus (Asteraceae) in Central Europe and adjacent areas. Plant Systematics and Evolution. 2012;298:1463–1482.

Pečinka A, Suchánková P, Lysák MA, Trávníček B, Doležel J. Nuclear DNA content variation among Central European Koeleria taxa. Annals of Botany. 2006;98:117–122. PubMed PMC

Pellicer J, Fay MF, Leitch IJ. The largest eukaryotic genome of them all? Botanical Journal of the Linnean Society. 2010;164:10–15.

Peres-Neto PR, Jackson DA. How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia. 2000;129:169–178. PubMed

Rangel TF, Diniz-Filho JAF, Bini LM. SAM: a comprehensive application for spatial analysis in macroecology. Ecography. 2010;33:1–5.

Rejmánek M. A theory of seed plant invasiveness: the first sketch. Biological Conservation. 1996;78:171–181.

Šafářová L, Duchoslav M. Cytotype distribution in mixed populations of polyploid Allium oleraceum measured at a microgeographic scale. Preslia. 2010;82:107–126.

Šafářová L, Duchoslav M, Jandová M, Krahulec F. Allium oleraceum in Slovakia: cytotype distribution and ecology. Preslia. 2011;83:513–527.

Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology. 2007;4(11) http://dx.doi.org/10.1186/1742-9994-4-11 . PubMed PMC

Slovák M, Vít P, Urfus T, Suda J. Complex pattern of genome size variation in a polymorphic member of the Asteraceae. Journal of Biogeography. 2009;36:372–384.

Šmarda P, Bureš P. Intraspecific DNA content variability in Festuca pallens on different geographical scales and ploidy levels. Annals of Botany. 2006;98:665–678. PubMed PMC

Šmarda P, Bureš P. Understanding intraspecific variation in genome size in plants. Preslia. 2010;82:41–61.

Šmarda P, Bureš P, Horová L, Rotreklová O. Intrapopulation genome size dynamics in Festuca pallens. Annals of Botany. 2008a;102:599–607. PubMed PMC

Šmarda P, Bureš P, Horová L. Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction. Annals of Botany. 2008b;101:421–433. PubMed PMC

Staňková H. Population genetics of the polyploid complex Allium oleraceum in the Czech Republic. Olomouc, Czech Republic: Department of Botany, Faculty of Science, Palacký University; 2005. MSc thesis.

Stearn WT. In: Allium L. In. Tutin TG, Heywood VH, Burges NA, et al., editors. Cambridge: Cambridge University Press; 1980. pp. 49–69. Flora Europaea 5.

Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F. Genome size variation and species relationships in Hieracium sub-genus Pilosella (Asteraceae) as inferred by flow cytometry. Annals of Botany. 2007;100:1323–1335. PubMed PMC

Swift HH. The constancy of desoxyribose nucleic acid in plant nuclei. Proceedings of the National Academy of Sciences. 1950;36:643–654. PubMed PMC

Veselý P, Bureš P, Šmarda P, Pavlíček T. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany. 2012;109:65–75. PubMed PMC

Weiss-Schneeweiss H, Greilhuber J, Schneeweiss GM. Genome size evolution in holoparasitic Orobanche (Orobanchaceae) and related genera. American Journal of Botany. 2006;93:148–156. PubMed

Wendel J. Genome evolution in polyploids. Plant Molecular Biology. 2000;42:225–249. PubMed

New estimates and synthesis of chromosome numbers, ploidy levels and genome size variation in Allium sect. Codonoprasum: advancing our understanding of the unresolved diversification and evolution of this section

Diploid and tetraploid cytotypes of the flagship Cape species Dicerothamnus rhinocerotis (Asteraceae): variation in distribution, ecological niche, morphology and genetics

Intricate Distribution Patterns of Six Cytotypes of Allium oleraceum at a Continental Scale: Niche Expansion and Innovation Followed by Niche Contraction With Increasing Ploidy Level

Molecular and Cytogenetic Study of East African Highland Banana

Evolutionary and Taxonomic Implications of Variation in Nuclear Genome Size: Lesson from the Grass Genus Anthoxanthum (Poaceae)