Nutrient reserves may allow for genome size increase: evidence from comparison of geophytes and their sister non-geophytic relatives

. 2013 Oct ; 112 (6) : 1193-200. [epub] 20130819

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23960044

BACKGROUND AND AIMS: The genome size of an organism is determined by its capacity to tolerate genome expansion, given the species' life strategy and the limits of a particular environment, and the ability for retrotransposon suppression and/or removal. In some giant-genomed bulb geophytes, this tolerance is explained by their ability to pre-divide cells in the dormant stages or by the selective advantage of larger cells in the rapid growth of their fleshy body. In this study, a test shows that the tendency for genome size expansion is a more universal feature of geophytes, and is a subject in need of more general consideration. METHODS: Differences in monoploid genome sizes were compared using standardized phylogenetically independent contrasts in 47 sister pairs of geophytic and non-geophytic taxa sampled across all the angiosperms. The genome sizes of 96 species were adopted from the literature and 53 species were newly measured using flow cytometry with propidium iodide staining. KEY RESULTS: The geophytes showed increased genome sizes compared with their non-geophytic relatives, regardless of the storage organ type and regardless of whether or not vernal geophytes, polyploids or annuals were included in the analyses. CONCLUSIONS: The universal tendency of geophytes to possess a higher genome size suggests the presence of a universal mechanism allowing for genome expansion. It is assumed that this is primarily due to the nutrient and energetic independence of geophytes perhaps allowing continuous synthesis of DNA, which is known to proceed in the extreme cases of vernal geophytes even in dormant stages. This independence may also be assumed as a reason for allowing large genomes in some parasitic plants, as well as the nutrient limitation of small genomes of carnivorous plants.

Zobrazit více v PubMed

Adamec L. Ecophysiological look at plant carnivory: why are plants carnivorous? In. In: Seckbach J, Dubinsky Z, editors. All flesh is grass. Cellular origin, life in extreme habitats and astrobiology. Berlin: Springer-Verlag; 2011. pp. 455–489.

Andersson L, Andersson S. A molecular phylogeny of Tropaeolaceae and its systematic implications. Taxon. 2000;49:721–736.

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

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

Bendiksby M, Thorbek L, Scheen AC, Lindqvist C, Ryding O. An updated phylogeny and classification of Lamiaceae subfamily Lamioideae. Taxon. 2011;60:471–484.

Bennett MD. The duration of meiosis. Proceedings of the Royal Society B: Biological Sciences. 1971;178:259–275.

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

Bennett MD, Leitch IJ. Plant DNA C-values Database (release 6·0, December 2012) 2012 http://data.kew.org/cvalues/

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

Blattner FR. Phylogenetic analysis of Hordeum (Poaceae) as inferred by nuclear rDNA ITS sequences. Molecular Phylogenetics and Evolution. 2004;33:289–299. PubMed

Carlsen T, Bleeker W, Hurka H, Elven R, Hochmann C. Biogeography and phylogeny of Cardamine (Brassicaceae) Annals of the Missouri Botanical Garden. 2009;96:215–236.

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

Dafni A, Cohen D, Noy-Meir I. Life-cycle variation in geophytes. Annals of the Missouri Botanical Garden. 1981;68:652–660.

Doležel J, Greilhuber J. Nuclear genome size: are we getting closer? Cytometry. 2010;77A:635–642. PubMed

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

Ehrendorfer F, Samuel R. Contributions to a molecular phylogeny and systematics of Anemone and related genera (Ranunculaceae–Anemoninae) Acta Phytotaxonomica Sinica. 2001;39:293–307.

Ellison AM. Nutrient limitation and stoichiometry of carnivorous plants. Plant Biology. 2006;8:740–747. PubMed

Fawcett JA, Van de Peer Y, Maere S. Significance and biological consequences of polyploidization in land plant evolution. In: Leitch IJ, Greilhuber J, Doležel J, Wendel J, editors. Plant genome diversity volume 2: physical structure, behaviour and evolution of plant genomes. Wien: Springer-Verlag; 2013. pp. 277–293.

Fedorov AA. Chromosome numbers of flowering plants. Leningrad: Nauka; 1969.

Felsenstein J. Phylogenies and the comparative method. American Naturalist. 1985;125:1–15. PubMed

Forrest LL, Hughes M, Hollingsworth PM. A phylogeny of Begonia using nuclear ribosomal sequence data and morphological characters. Systematic Botany. 2005;30:671–682.

Frajman B, Schönswetter P. Giants and dwarfs: molecular phylogenies reveal multiple origins of annual spurges within Euphorbia subg. Esula. Molecular Phylogenetics and Evolution. 2011;61:413–424. PubMed

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

Garland T, Harvey PH, Ives AR. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology. 1992;41:18–32.

Gauthier MPL, Barabe D, Bruneau A. Molecular phylogeny of the genus Philodendron (Araceae): delimitation and infrageneric classification. Botanical Journal of the Linnean Society. 2008;156:13–27.

Gleissberg S, Kadereit JW. Evolution of leaf morphogenesis: evidence from developmental and phylogenetic data in Papaveraceae. International Journal of Plant Sciences. 1999;160:787–794.

Goldblatt P, Johnson DE, editors. Index to plant chromosome numbers (September 2012) 1979–onwards. Missouri Botanical Garden, St Louis. http://www.tropicos.org/Project/IPCN .

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. Chromosomes of the monocotyledons (general aspects) In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ, editors. Monocotyledons: systematics and evolution. Kew: Royal Botanic Garden; 1995. pp. 379–414.

Greilhuber J, Leitch IJ. Genome size and the phenotype. In: Leitch IJ, Greilhuber J, Doležel J, Wendel J, editors. Plant genome diversity volume 2: physical structure, behaviour and evolution of plant genomes. Wien: Springer-Verlag; 2013. pp. 323–344.

Greilhuber J, Doležel J, Lysák M, 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, Miller 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

Grime JP. Prediction of weed and crop response to climate based upon measurements of nuclear DNA content. Aspects of Applied Biology. 1983;4:87–98.

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

Hibberd JM, Jeschke WD. Solute flux into parasitic plants. Journal of Experimental Botany. 2001;52:2043–2049. PubMed

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

Hörandl E, Paun A, Johansson JT, et al. Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Molecular Phylogenetics and Evolution. 2005;36:305–327. PubMed

Huang J, Corke H, Sun M. Highly polymorphic AFLP markers as a complementary tool to ITS sequences in assessing genetic diversity and phylogenetic relationships of sweetpotato (Ipomoea batatas (L.) Lam.) and its wild relatives. Genetic Resources and Crop Evolution. 2002;49:541–550.

International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature. 2004;431:931–945. PubMed

International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature. 2005;436:793–800. PubMed

Janssens S, Geuten K, Juan YM, Song Y, Küpfer P, Smets E. Phylogenetics of Impatiens and Hydrocera (Balsaminaceae) using chloroplast atpB-rbcL spacer sequences. Systematic Botany. 2006;31:171–180.

Karagatzides JD, Butler JL, Ellison AM. The pitcher plant Sarracenia purpurea can directly acquire organic nitrogen and short-circuit the inorganic nitrogen cycle. PLoS One. 2009;4:1–9. PubMed PMC

Kejnovský E, Hawkins JS, Feschotte C. Plant transposable elements: biology and evolution. In: Wendel J, Greilhuber J, Doležel J, Leitch IJ, editors. Plant genome diversity volume 1: plant genomes, their residents, and their evolutionary dynamics. Wien: Springer-Verlag; 2012. pp. 17–34.

Kenicer GJ, Kajita T, Pennington RT, Murata J. Systematics and biogeography of Lathyrus (Leguminosae) based on internal transcribed spacer and cpDNA sequence data. American Journal of Botany. 2005;92:1199–1209. PubMed

Kim JD, Kim SH, Kim CH, Jansen RK. Phylogeny of Berberidaceae based on sequences of the chloroplast gene ndhF. Biochemical Systematics and Ecology. 2004;32:291–301.

Kim JH, Kim DK, Forest F, Fay MF, Chase MW. Molecular phylogenetics of Ruscaceae sensu lato and related families (Asparagales) based on plastid and nuclear DNA sequences. Annals of Botany. 2010;106:775–790. PubMed PMC

Kocyan A, Zhang LB, Schaefer H, Renner SS. A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Molecular Phylogenetics and Evolution. 2007;44:553–577. PubMed

Krähenbühl M, Juan YM, Küpfer P. Chromosome and breeding system evolution of the genus Mercurialis (Euphorbiaceae): implications of ITS molecular phylogeny. Plant Systematics and Evolution. 2002;234:155–169.

Kubát K, Hrouda L, Chrtek J Jr, Kaplan Z, Kirschner J, Štěpánek J, editors. Key to the Flora of the Czech Republic. Praha: Academia; 2002.

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

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

Leitch IJ, Soltis DE, Soltis PS, Bennett MD. Evolution of DNA amounts across land plants (Embryophyta) Annals of Botany. 2005;95:207–217. PubMed PMC

Lifante ZD. Pollen morphology of Asphodelus L. (Asphodelaceae): taxonomic and phylogenetic inferences at the infrageneric level. Grana. 1996;35:24–32.

Moore BR, Donoghue MJ. A Bayesian approach for evaluating the impact of historical events on rates of diversification. Proceedings of the National Academy of Sciences, USA. 2009;106:4307–4312. PubMed PMC

Muschner VC, Lorenz AP, Cervi AC, et al. A first molecular phylogenetic analysis of Passiflora (Passifloraceae) American Journal of Botany. 2003;90:1229–1238. PubMed

Nie ZL, Sun H, Chen ZD, Meng Y, Manchester SR, Wen J. Molecular phylogeny and biogeographic diversification of Parthenocissus (Vitaceae) disjunct between Asia and North America. American Journal of Botany. 2010;97:1342–1353. PubMed

Oberlander KC. Molecular systematic study of southern African Oxalis (Oxalidaceae). Stellenbosch University: South Africa; 2009. PhD thesis.

Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM. The mode and tempo of genome size evolution in eukaryotes. Genome Research. 2007;17:594–601. PubMed PMC

Otto F. DAPI staining of fixed cells for high resolution flow cytometry of nuclear DNA. Methods in Cell Biology. 1990;33:105–11. PubMed

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

Petrov AD. Evolution of genome size: new approaches to an old problem. Trends in Genetics. 2001;17:23–28. PubMed

Piegu B, Guyot R, Picault N, et al. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Research. 2006;16:1262–1269. PubMed PMC

Ruiters C, McKenzie B. Seasonal allocation and efficiency patterns of biomass and resources in the perennial geophyte Sparaxis grandiflora subspecies fimbriata (Iridaceae) in lowland coastal fynbos, South Africa. Annals of Botany. 1994;74:633–646.

Sennblad B, Bremer B. Classification of Apocynaceae s.l. according to a new approach combining Linnaean and phylogenetic taxonomy. Systematic Biology. 2002;51:389–409. PubMed

Soltis DE, Albert VA, Leebens-Mack J, et al. Polyploidy and angiosperm diversifications. American Journal of Botany. 2009;96:336–348. PubMed

Stebbins GL. Cytological characteristics associated with the different growth habits in the Dicotyledons. American Journal of Botany. 1938;25:180–198.

Szinay D, Wijnker E, van den Berg R, Visser RGF, de Jong H, Bai Y. Chromosome evolution in Solanum traced by cross-species BAC-FISH. New Phytologist. 2012;195:688–698. PubMed

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

Šmarda P, Hejcman M, Březinová A, et al. Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilisation experiment. New Phytologist. 2013 in press. doi: 10.1111/nph.12399. PubMed

Tam SM, Boyce PC, Upson TM, et al. Intergeneric and infrafamilial phylogeny of subfamily Monsteroideae (Araceae) revealed by chloroplast trnL-F sequences. American Journal of Botany. 2004;91:490–498. PubMed

Timme RE, Simpson BB, Linder CR. High-resolution phylogeny for Helianthus (Asteraceae) using the 18S–26S ribosomal DNA external transcribed spacer. American Journal of Botany. 2007;94:1837–1852. PubMed

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

Voltz SM, Renner SS. Hybridization, polyploidy, and evolutionary transitions between monoecy and dioecy in Bryonia (Cucurbitaceae) American Journal of Botany. 2008;95:1297–1306. PubMed

Webb C, Ackerly D, Kembel S. Phylocom: software for the analysis of phylogenetic community structure and character evolution. 2011 http://phylodiversity.net/phylocom/ PubMed

Zonneveld BJM. New record holders for maximum genome size in Eudicots and Monocots. Journal of Botany. 2010;2010:527357.

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace