Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
18158307
PubMed Central
PMC2701825
DOI
10.1093/aob/mcm307
PII: mcm307
Knihovny.cz E-zdroje
- MeSH
- Festuca genetika MeSH
- fylogeneze MeSH
- genom rostlinný * MeSH
- molekulární evoluce * MeSH
- polyploidie MeSH
- retroelementy MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- retroelementy MeSH
BACKGROUND AND AIMS: Plant evolution is well known to be frequently associated with remarkable changes in genome size and composition; however, the knowledge of long-term evolutionary dynamics of these processes still remains very limited. Here a study is made of the fine dynamics of quantitative genome evolution in Festuca (fescue), the largest genus in Poaceae (grasses). METHODS: Using flow cytometry (PI, DAPI), measurements were made of DNA content (2C-value), monoploid genome size (Cx-value), average chromosome size (C/n-value) and cytosine + guanine (GC) content of 101 Festuca taxa and 14 of their close relatives. The results were compared with the existing phylogeny based on ITS and trnL-F sequences. KEY RESULTS: The divergence of the fescue lineage from related Poeae was predated by about a 2-fold monoploid genome and chromosome size enlargement, and apparent GC content enrichment. The backward reduction of these parameters, running parallel in both main evolutionary lineages of fine-leaved and broad-leaved fescues, appears to diverge among the existing species groups. The most dramatic reductions are associated with the most recently and rapidly evolving groups which, in combination with recent intraspecific genome size variability, indicate that the reduction process is probably ongoing and evolutionarily young. This dynamics may be a consequence of GC-rich retrotransposon proliferation and removal. Polyploids derived from parents with a large genome size and high GC content (mostly allopolyploids) had smaller Cx- and C/n-values and only slightly deviated from parental GC content, whereas polyploids derived from parents with small genome and low GC content (mostly autopolyploids) generally had a markedly increased GC content and slightly higher Cx- and C/n-values. CONCLUSIONS: The present study indicates the high potential of general quantitative characters of the genome for understanding the long-term processes of genome evolution, testing evolutionary hypotheses and their usefulness for large-scale genomic projects. Taken together, the results suggest that there is an evolutionary advantage for small genomes in Festuca.
Zobrazit více v PubMed
Ahn S, Tanksley SD. Comparative linkage maps of the rice and maize genomes. Proceedings of the National Academy of Sciences of the USA. 1993;90:7980–7984. PubMed PMC
Ainscough MM, Barker CM, Stace CA. Natural hybrids between Festuca and species of Vulpia section Vulpia. Watsonia. 1986;16:143–151.
Alm V, Fang C, Busso CS, Devos KM, Vollan K, Grieg Z, Rognli OA. A linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species. Theoretical and Applied Genetics. 2003;180:25–40. PubMed
Ammiraju JSS, Luo MZ, Goicoechea JL, Wang WM, Kudrna D, Mueller C, et al. The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. Genome Research. 2006;16:140–147. PubMed PMC
Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796–815. PubMed
Bancheva S, Greilhuber J. Genome size in Bulgarian Centaurea s.l. (Asteraceae) Plant Systematics and Evolution. 2006;257:95–117.
Barow M, Meister A. Lack of correlation between AT frequency and genome size in higher plants and the effect of nonrandomness of base sequences on dye binding. Cytometry. 2002;47:1–7. PubMed
Basak S, Ghosh TC. On the origin of genomic adaptation at high temperature for prokaryotic organisms. Biochemical and Biophysical Research Communications. 2005;330:629–632. PubMed
Bennett MD, Leitch IJ. Angiosperm DNA C-values database. 2004 www.rbgkew.org.uk/cval/homepage.html. (release 5·0, December 2004)
Bennetzen JL. Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica. 2002;115:29–36. PubMed
Bennetzen JL, Ma J, Devos KM. Mechanisms of recent genome size variation in flowering plants. Annals of Botany. 2005;95:127–132. PubMed PMC
Bernardi G. Isochores and the evolutionary dynamics of vertebrates. Gene. 2000;a 241:3–17. PubMed
Bernardi G. The compositional evolution of vertebrate genomes. Gene. 2000;a 259:31–43. PubMed
Bureš P, Wang Y-F, Horová L, Suda J. Genome size variation in Central European species of Cirsium (Compositae) and their natural hybrids. Annals of Botany. 2004;94:353–363. PubMed PMC
Caetano-Anollés G. Evolution of genome size in the grasses. Crop Science. 2005;45:1809–1816.
Carels N, Bernardi G. Two classes of genes in plants. Genetics. 2000;154:1819–1825. PubMed PMC
Catalán P, Torrecilla P, López Rodríguez JA, Olmstead RG. Phylogeny of festucoid grasses of subtribe Loliinae and allies (Poeae, Pooideae) inferred from ITS and trnL-F sequences. Molecular Phyogenetics and Evolution. 2004;31:517–541. PubMed
Clayton WD, Harman KT, Williamson H. onwards. World Grass Species, Descriptions, Identification and Information Retrieval. [(accessed 3 January 2007)];2002 http://www.kew.org/data/grasses–db.html .
Doležel J, Greilhuber J, Lucretti S, Meister A, Lysák MA, Nardi L, et al. Plant genome size estimation by flow cytometry: inter-laboratory comparison. Annals of Botany. 1998;82(Suppl. A):17–26.
Dubcovsky J, Martínez A. Distribución geográfica de los niveles de ploidía en Festuca. Parodiana. 1992;7:91–99.
Eyre-Walker A, Hurst LD. The evolution of isochores. Nature Reviews Genetics. 2001;2:549–555. PubMed
Feldman M, Liu B, Segal G, Abbo S, Levy AA, Vega JM. Rapid elimination of low-copy DNA sequences in polyploid wheat, a possible mechanism for differentiation of homoeologous chromosomes. Genetics. 1997;147:1381–1387. PubMed PMC
Feuillet C, Keller B. Comparative genomics in the Grass family: molecular characterisation of grass genome structure and evolution. Annals of Botany. 2002;89:3–10. PubMed PMC
Gaut BS. Evolutionary dynamics of grass genome. New Phytologist. 2002;154:15–28.
Gaut BS, Doebley JF. DNA sequence evidence for the segmental allotetraploid origin of maize. Proceedings of the National Academy of Sciences of the USA. 1997;94:6809–6814. PubMed PMC
Gaut BS, Tredway LP, Kubik C, Gaut RL, Meyer W. Phylogenetic relationships and genetic diversity among members of the Festuca-Lolium complex (Poaceae) based on ITS sequence data. Plant Systematics and Evolution. 2000;224:33–53.
Gregory TR. Synergy between sequence and size in large-scale genomics. Nature Reviews Genetics. 2005;6:699–708. PubMed
Greilhuber J, Doležel J, Lysák MA, Bennett MD. The origin, evolution and proposed stabilisation of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Annals of Botany. 2005;95:255–260. PubMed PMC
Haberer G, Young S, Bharti AK, Gundlach H, Raymond C, Fuks G, et al. Structure and architecture of the maize genome. Plant Physiology. 2005;139:1612–1624. PubMed PMC
Hawkins JS, Kim H-R, Nason JD, Wing RA, Wendel JF. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Research. 2006;16:1252–1261. PubMed PMC
Hunziker JH, Stebbins GL. Chromosomal evolution in the Gramineae. In: Soderstrom TR, Hilu KW, Campbell CS, Barkworth ME, editors. Grass systematics and evolution. Washington, DC: Smithsonian Institution Press; 1987. pp. 178–187.
Ilic K, SanMiguel PJ, Bennetzen JL. A complex history of rearrangement in an orthologous region of the maize, sorghum and rice genomes. Proceedings of the National Academy of Sciences of the USA. 2003;100:12265–12270. PubMed PMC
International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature. 2005;436:793–800. PubMed
Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ. Evolution of genome size in Brassicaceae. Annals of Botany. 2005;95:229–235. PubMed PMC
Kellogg EA. Relationships of cereal crops and other grasses. Proceedings of the National Academy of Sciences of the USA. 1998;95:2005–2010. PubMed PMC
Kellogg EA, Bennetzen JL. The evolution of nuclear genome structure in seed plants. American Journal of Botany. 2004;91:1709–1725. PubMed
Kerguélen M, Plonka F. Les Festuca de la Flore de la France (Corse complice) Buletin de la Société Botanique du Centre-Ouest. 1989;10:1–368.
King GJ, Ingrouille MJ. Genome heterogenity and classification of the Poaceae. New Phytologist. 1987;107:633–644.
Knight CA, Molinari NA, Petrov DA. The large genome constraint hypothesis, evolution, ecology and phenotype. Annals of Botany. 2005;95:177–190. PubMed PMC
Kuhl JC, Cheung F, Yuan Q, Martin W, Zewdie Y, McCallum J, et al. A unique set of 11,008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders Asparagales and Poales. The Plant Cell. 2004;16:114–125. PubMed PMC
Kumar A, Bennetzen JL. Plant retrotransposons. Annual Review of Genetics. 1999;33:479–532. PubMed
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
Li W, Zhang P, Fellers JP, Friebe B, Gill BS. Sequence composition, organisation and evolution of the core Triticeae genome. The Plant Journal. 2004;40:500–511. PubMed
Loureiro J, Kopecký D, Castro S, Santos C, Silveira P. Flow cytometric and cytogenetic analyses of Iberian Peninsula Festuca spp. Plant Systematics and Evolution. 2007;269:89–105.
Lumaret R, Bowman CM, Dyer TA. Autopolyploidy in Dactylis glomerata L. – further evidence from studies of chloroplast DNA variation. Theoretical and Applied Genetics. 1989;78:393–399. PubMed
Ma J, Devos KM, Bennetzen JL. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Research. 2004;14:860–869. PubMed PMC
Meister A, Barow M. DNA base composition of plant genomes. In: Doležel J, Greilhuber J, Suda J, editors. Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA; 2007. pp. 177–215.
Messing J, Dooner H. Organisation and variability of the maize genome. Current Opinion in Plant Biology. 2006;9:157–163. PubMed
Messing J, Bharti AK, Karlowski WM, Grundlach H, Kim HR, Yu Y, et al. Sequence composition and genome organisation of maize. Proceedings of the National Academy of Sciences of the USA. 2004;101:14349–14354. PubMed PMC
Meyers BC, Tungey SV, Morgante M. Abundance, distribution and transcriptional activity of repetitive elements in the maize genome. Genome Research. 2001;11:1660–1676. PubMed PMC
Musto H, Naya H, Zavala A, Romeo H, Alvarez-Valín F, Bernardi G. Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Letters. 2004;573:73–77. PubMed
Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S, et al. Comparative complete genome sequence analysis of the amino acid replacements responsible for thermostability of Corynebacterium efficiens. Genome Research. 2003;13:1572–1579. PubMed PMC
Noma K, Nakajima R, Ohtsubo H, Ohtsubo E. RIRE1, a retrotransposon from wild rice Oryza australiensis. Genes and Genetic Systems. 1997;72:131–140. PubMed
Otto F. DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Crissman HA, Darzynkiewicz Z, editors. Methods in cell biology. Vol. 33. New York, NY: Academic Press; 1990. pp. 105–110. Flow cytometry. PubMed
Ozkan H, Levy AA, Feldman M. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. The Plant Cell. 2001;13:1735–1747. PubMed PMC
Ozkan H, Tuna M, Arumuganathan K. Nonadditive changes in genome size during allopolyploidisation in the wheat (Aegilops-Triticum) group. Journal of Heredity. 2003;94:260–264. PubMed
Pasakinskiene I, Anamthawat-Jonsson K, Humphreys MW, Paplauskiene V, Jones RN. New molecular evidence on genome relationships and chromosome identification in fescue (Festuca) and ryegrass (Lolium) Heredity. 1998;81:659–665.
Paterson AH, Freeling M, Sasaki T. Grains of knowledge: genomics of model cereals. Genome Research. 2005;15:1643–1650. PubMed
Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C. Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. The Plant Journal. 2006;48:463–474. PubMed
Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, et al. Doubling genome size without polyploidization, dynamics of retrotransposition-driven genomic expansion in Oryza australensis, a wild relative of rice. Genome Research. 2006;16:1262–1269. PubMed PMC
Price HJ, Dillon SL, Hodnett G, Rooney WL, Ross L, Johnston JS. Genome evolution in the genus Sorghum (Poaceae) Annals of Botany. 2005;95:219–227. PubMed PMC
Rieseberg LH, Van Fossen C, Desrochers AM. Hybrid speciation accompanied by genomic reorganisation in wild sunflowers. Nature. 1995;375:313–316.
SanMiguel P, Bennetzen JL. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Annals of Botany. 1998;82:37–44.
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. The paleontology of intergene retrotransposons of maize. Nature Genetics. 1998;20:43–45. PubMed
Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. The Plant Cell. 2001;13:1749–1759. PubMed PMC
Šmarda P. DNA ploidy levels and intraspecific DNA content variability in Romanian fescues (Festuca L, Poaceae), measured in fresh and herbarium material. Folia Geobotanica. 2006;41:417–432.
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, Kočí K. Chromosome number variability in Central European members of the Festuca ovina and F. pallens groups (sect Festuca) Folia Geobotanica. 2003;38:65–95.
Šmarda P, Stančík D. Ploidy level variability in South American fescues (Festuca L, Poaceae), use of flow cytometry in up to 5½-year-old caryopses and herbarium specimens. Plant Biology. 2006;8:73–80. PubMed
Šmarda P, Horová L, Bureš P. Random distribution pattern and non-adaptivity of genome size in a highly variable population of Festuca pallens. Annals of Botany. 2007;100:141–150. PubMed PMC
Stace CA. Plant taxonomy and biosystematics – does DNA provide all the answers? Taxon. 2005;54:999–1007.
Suda J, Kyncl T, Jarolímová V. Genome size variation in Macaronesian angiosperms: forty percent of the Canarian endemic flora completed. Plant Systematics and Evolution. 2005;252:215–238.
Torrecilla P, Catalán P. Phylogeny of broad-leaved and fine-leaved Festuca lineages (Poaceae) based on nuclear ITS sequences. Systematic Botany. 2002;27:241–251.
Torrecilla P, López-Rodríguez JA, Catalán P. Phylogenetic relationships of Vulpia and related genera (Poeae, Poaceae) based on analysis of ITS and trnL-F sequences. Annals of the Missouri Botanical Garden. 2004;91:124–158.
Turcotte K, Srinivasan S, Burelu T. Survey of transposable elements from rice genomic sequences. The Plant Journal. 2001;25:169–179. PubMed
Uozu S, Ikehashi H, Ohmido N, Ohtsubo H, Ohtsubo E, Fukui K. Repetitive sequences: cause for variation in genome size and chromosome morphology in the genus Oryza. Plant Molecular Biology. 1997;35:791–799. PubMed
Vitte C, Panaud O. LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenetic and Genome Research. 2005;110:91–107. PubMed
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
Wong GK-S, Wang J, Tao L, Tan J, Zhang J-G, Passey DA, Yu J. Compositional gradients in Gramineae genes. Genome Research. 2002;12:851–856. PubMed PMC
Závesky L, Jarolímová V, Štěpánek J. Nuclear DNA content variation within the genus Taraxacum (Asteraceae) Folia Geobotanica. 2005;40:91–104.
Zhang R, Zhang C-T. Isochore structures in the genome of plant Arabidopsis thaliana. Journal of Molecular Evolution. 2004;59:227–238. PubMed
Zoubak S, Clay O, Bernardi G. The gene distribution of the human genome. Gene. 1996;174:95–102. PubMed
New estimates of genome size in Orthoptera and their evolutionary implications
Chromosome size matters: genome evolution in the cyperid clade
Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae)
Ecological and evolutionary significance of genomic GC content diversity in monocots
Genome size and DNA base composition of geophytes: the mirror of phenology and ecology?
Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis
Intrapopulation genome size dynamics in Festuca pallens