Ecological and evolutionary significance of genomic GC content diversity in monocots

. 2014 Sep 30 ; 111 (39) : E4096-102. [epub] 20140915

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25225383

Genomic DNA base composition (GC content) is predicted to significantly affect genome functioning and species ecology. Although several hypotheses have been put forward to address the biological impact of GC content variation in microbial and vertebrate organisms, the biological significance of GC content diversity in plants remains unclear because of a lack of sufficiently robust genomic data. Using flow cytometry, we report genomic GC contents for 239 species representing 70 of 78 monocot families and compare them with genomic characters, a suite of life history traits and climatic niche data using phylogeny-based statistics. GC content of monocots varied between 33.6% and 48.9%, with several groups exceeding the GC content known for any other vascular plant group, highlighting their unusual genome architecture and organization. GC content showed a quadratic relationship with genome size, with the decreases in GC content in larger genomes possibly being a consequence of the higher biochemical costs of GC base synthesis. Dramatic decreases in GC content were observed in species with holocentric chromosomes, whereas increased GC content was documented in species able to grow in seasonally cold and/or dry climates, possibly indicating an advantage of GC-rich DNA during cell freezing and desiccation. We also show that genomic adaptations associated with changing GC content might have played a significant role in the evolution of the Earth's contemporary biota, such as the rise of grass-dominated biomes during the mid-Tertiary. One of the major selective advantages of GC-rich DNA is hypothesized to be facilitating more complex gene regulation.

Zobrazit více v PubMed

Flagel LE, Blackman BK. The first ten years of plant genome sequencing and prospects for the next decade. In: Wendel JF, Greilhuber J, Doležel J, Leitch IJ, editors. Plant Genome Diversity. Vol 1. Vienna: Springer; 2012. pp. 1–15.

Galbraith DW, Bennetzen JF, Kellogg EA, Pires JC, Soltis PS. The genomes of all angiosperms: A call for a coordinated global census. J Bot. 2011 doi: 10.1155/2011/646198. DOI

Stackebrandt E, Liesack W. Nucleic acids and classification. In: Goodfellow M, O’Donnell AG, editors. Handbook of New Bacterial Systematics. London: Academic; 1993. pp. 151–194.

Bentley SD, Parkhill J. Comparative genomic structure of prokaryotes. Annu Rev Genet. 2004;38:771–792. PubMed

Foerstner KU, von Mering C, Hooper SD, Bork P. Environments shape the nucleotide composition of genomes. EMBO Rep. 2005;6(12):1208–1213. PubMed PMC

Mann S, Chen YP. Bacterial genomic G+C composition-eliciting environmental adaptation. Genomics. 2010;95(1):7–15. PubMed

Wu H, Zhang Z, Hu S, Yu J. On the molecular mechanism of GC content variation among eubacterial genomes. Biol Direct. 2012;7:2. PubMed PMC

Eyre-Walker A, Hurst LD. The evolution of isochores. Nat Rev Genet. 2001;2(7):549–555. PubMed

Bernardi G. The neoselectionist theory of genome evolution. Proc Natl Acad Sci USA. 2007;104(20):8385–8390. PubMed PMC

Costantini M, Cammarano R, Bernardi G. The evolution of isochore patterns in vertebrate genomes. BMC Genomics. 2009;10:146. PubMed PMC

Šmarda P, Bureš P. The variation of base composition in plant genomes. In: Wendel F, Greilhuber J, Doležel J, Leitch IJ, editors. Plant Genome Diversity. Vol 1. Vienna: Springer; 2012. pp. 209–235.

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):1–7. PubMed

Meister A, Barow M. In: Flow Cytometry with Plant Cells. Analysis of Genes, Chromosomes, and Genomes. Dolezel J, Greilhuber J, Suda J, editors. Weinheim, Germany: Wiley-VCH; 2007. pp. 177–215.

Šmarda P, Bureš P, Horová L, Foggi B, Rossi G. Genome size and GC content evolution of Festuca: Ancestral expansion and subsequent reduction. Ann Bot (Lond) 2008;101(3):421–433. PubMed PMC

Šmarda P, Bureš P, Šmerda J, Horová L. Measurements of genomic GC content in plant genomes with flow cytometry: A test for reliability. New Phytol. 2012;193(2):513–521. PubMed

Veselý P, Bureš P, Šmarda P, Pavlícek T. Genome size and DNA base composition of geophytes: The mirror of phenology and ecology? Ann Bot (Lond) 2012;109(1):65–75. PubMed PMC

Lipnerová I, Bureš P, Horová L, Šmarda P. Evolution of genome size in Carex (Cyperaceae) in relation to chromosome number and genomic base composition. Ann Bot (Lond) 2013;111(1):79–94. PubMed PMC

Veleba A, et al. Genome size and genomic GC content evolution in the miniature genome-sized family Lentibulariaceae. New Phytol. 2014;203(1):22–28. PubMed

Yakovchuk P, Protozanova E, Frank-Kamenetskii MD. Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 2006;34(2):564–574. PubMed PMC

Biro JC. Correlation between nucleotide composition and folding energy of coding sequences with special attention to wobble bases. Theor Biol Med Model. 2008;5:14. PubMed PMC

Nishio Y, et al. Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res. 2003;13(7):1572–1579. PubMed PMC

Musto H, et al. Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun. 2006;347(1):1–3. PubMed

Galtier N, Piganeau G, Mouchiroud D, Duret L. GC-content evolution in mammalian genomes: The biased gene conversion hypothesis. Genetics. 2001;159(2):907–911. PubMed PMC

Vinogradov AE. DNA helix: The importance of being GC-rich. Nucleic Acids Res. 2003;31(7):1838–1844. PubMed PMC

Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. Molecular basis of base substitution hotspots in Escherichia coli. Nature. 1978;274(5673):775–780. PubMed

Pfeifer GP. Mutagenesis at methylated CpG sequences. In: Doerfler W, Böhm P, editors. DNA Methylation: Basic Mechanisms. Berlin: Springer; 2006. pp. 259–281. PubMed

Ossowski S, et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science. 2010;327(5961):92–94. PubMed PMC

Rocha EPC, Danchin A. Base composition bias might result from competition for metabolic resources. Trends Genet. 2002;18(6):291–294. PubMed

Salinas J, Matassi G, Montero LM, Bernardi G. Compositional compartmentalization and compositional patterns in the nuclear genomes of plants. Nucleic Acids Res. 1988;16(10):4269–4285. PubMed PMC

International Rice Genome Sequencing Project The map-based sequence of the rice genome. Nature. 2005;436(7052):793–800. PubMed

Schnable PS, et al. The B73 maize genome: Complexity, diversity, and dynamics. Science. 2009;326(5956):1112–1115. PubMed

Serres-Giardi L, Belkhir K, David J, Glémin S. Patterns and evolution of nucleotide landscapes in seed plants. Plant Cell. 2012;24(4):1379–1397. PubMed PMC

Lee KY. Studies on the base composition of higher plants. 1. Monocotyledons. BMB Rep. 1968;1(2):99–107.

Biswas SB, Sarkar AK. Deoxyribonucleic acid base composition of some angiosperms and its taxonomic significance. Phytochemistry. 1970;9(12):2425–2430.

Stromberg CAE. Evolution of grasses and grassland ecosystems. Annu Rev Earth Planet Sci. 2011;39:517–544.

Edwards EJ, et al. C4 Grasses Consortium The origins of C4 grasslands: Integrating evolutionary and ecosystem science. Science. 2010;328(5978):587–591. PubMed

Grass Phylogeny Working Group II New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 2012;193(2):304–312. PubMed

Franchi GG, Nepi M, Dafni A, Pacini E. Partially hydrated pollen: Taxonomic distribution, ecological and evolutionary significance. Plant Syst Evol. 2002;234(1-4):211–227.

Franchi GG, et al. Pollen and seed desiccation tolerance in relation to degree of developmental arrest, dispersal, and survival. J Exp Bot. 2011;62(15):5267–5281. PubMed

Angiosperm Phylogeny Group An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc. 2009;161(2):105–121.

Bureš P, et al. Correlation between GC content and genome size in plants. Cytometry A. 2007;71A(9):764.

Vinogradov AE. Genome size and GC-percent in vertebrates as determined by flow cytometry: The triangular relationship. Cytometry. 1998;31(2):100–109. PubMed

Bennetzen JL, Ma J, Devos KM. Mechanisms of recent genome size variation in flowering plants. Ann Bot (Lond) 2005;95(1):127–132. PubMed PMC

Grover CE, Wendel JF. Recent insights into mechanisms of genome size change in plants. J Bot. 2010 doi: 10.1155/2010/382732. DOI

SanMiguel P, Vitte C. The LTR-retrotransposons of maize. In: Bennetzen J, Hake S, editors. Handbook of Maize Genetics and Genomics. New York: Springer; 2009. pp. 307–327.

Bureš P, Zedek F, Marková M. Holocentric chromosomes. In: Leitch IJ, Greilhuber J, Doležel J, Wendel J, editors. Plant Genome Diversity. Vol 2. Vienna: Springer; 2013. pp. 187–208.

Brown TC, Jiricny J. Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells. Cell. 1988;54(5):705–711. PubMed

Wiens JJ, Donoghue MJ. Historical biogeography, ecology and species richness. Trends Ecol Evol. 2004;19(12):639–644. PubMed

Zanne AE, et al. Three keys to the radiation of angiosperms into freezing environments. Nature. 2014;506(7486):89–92. PubMed

Pearce RS. Plat freezing and damage. Ann Bot (Lond) 2001;87(4):417–424.

Beck EH, Heim R, Hansen J. Plant resistance to cold stress: Mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci. 2004;29(4):449–459. PubMed

Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T. Specific and unspecific responses of plants to cold and drought stress. J Biosci. 2007;32(3):501–510. PubMed

Katifori E, Alben S, Cerda E, Nelson DR, Dumais J. Foldable structures and the natural design of pollen grains. Proc Natl Acad Sci USA. 2010;107(17):7635–7639. PubMed PMC

Dafni A, Firmage D. Pollen viability and longevity: Practical, ecological and evolutionary implications. Plant Syst Evol. 2000;222(1-4):113–132.

Reddi CS, Raju NSN, Rao MVS. Pollination and seed set in tropical wetland grasses. Nord J Bot. 2010;28(3):354–365.

Franchi GG, Nepi M, Matthews ML, Pacini E. Anther opening, pollen biology and stigma receptivity in the long blooming species, Parietaria judaica L. (Urticaceae) Flora. 2007;202(2):118–127.

Tatarinova TV, Alexandrov NN, Bouck JB, Feldmann KA. GC3 biology in corn, rice, sorghum and other grasses. BMC Genomics. 2010;11:308. PubMed PMC

Zachos J, Pagani M, Sloan L, Thomas E, Billups K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science. 2001;292(5517):686–693. PubMed

Linder PH, Rudall PJ. Evolutionary history of Poales. Annu Rev Ecol Evol Syst. 2005;36:107–124.

Guo X, Bao J, Fan L. Evidence of selectively driven codon usage in rice: Implications for GC content evolution of Gramineae genes. FEBS Lett. 2007;581(5):1015–1021. PubMed

Rich A, Zhang S. Z-DNA: The long road to biological function. Nat Rev Genet. 2003;4(7):566–572. PubMed

Saenger W, Hunter WN, Kennard O. DNA conformation is determined by economics in the hydration of phosphate groups. Nature. 1986;324(6095):385–388. PubMed

Foloppe N, MacKerell AD., Jr Intrinsic conformational properties of deoxyribonucleosides: Implicated role for cytosine in the equilibrium among the A, B, and Z forms of DNA. Biophys J. 1999;76(6):3206–3218. PubMed PMC

Fuller W, Forsyth T, Mahendrasingam A. Water-DNA interactions as studied by X-ray and neutron fibre diffraction. Philos Trans R Soc Lond B Biol Sci. 2004;359(1448):1237–1247. 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. Ann Bot (Lond) 2005;95(1):255–260. PubMed PMC

Lengyel A, Chytrý M, Tichý L. Heterogeneity-constrained random resampling of phytosociological databases. J Veg Sci. 2011;22(1):175–183.

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25(15):1965–1978.

Paradis E, Claude J, Strimmer K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20(2):289–290. PubMed

R Development Core Team . R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2012.

Orme D. 2012. The Caper Package: Comparative Analysis of Phylogenetics and Evolution in R. Available at http://cran.r-project.org/web/packages/caper/vignettes/caper.pdf. Accessed March 23, 2013.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

G-quadruplexes in the evolution of hepatitis B virus

. 2023 Aug 11 ; 51 (14) : 7198-7204.

Complex patterns of ploidy in a holocentric plant clade (Schoenus, Cyperaceae) in the Cape biodiversity hotspot

. 2023 Feb 07 ; 131 (1) : 143-156.

Advances in Vertebrate (Cyto)Genomics Shed New Light on Fish Compositional Genome Evolution

. 2023 Jan 17 ; 14 (2) : . [epub] 20230117

Chromosome size matters: genome evolution in the cyperid clade

. 2022 Dec 31 ; 130 (7) : 999-1014.

Stoichiometry versus ecology: the relationships between genome size and guanine-cytosine content, and tissue nitrogen and phosphorus in grassland herbs

. 2022 Sep 06 ; 130 (2) : 189-197.

Reference standards for flow cytometric estimation of absolute nuclear DNA content in plants

. 2022 Sep ; 101 (9) : 710-724. [epub] 20210818

Substantial intraspecific genome size variation in golden-brown algae and its phenotypic consequences

. 2020 Oct 30 ; 126 (6) : 1077-1087.

Environmental pressures on stomatal size may drive plant genome size evolution: evidence from a natural experiment with Cape geophytes

. 2020 Jul 24 ; 126 (2) : 323-330.

Insights into the karyotype and genome evolution of haplogyne spiders indicate a polyploid origin of lineage with holokinetic chromosomes

. 2019 Feb 28 ; 9 (1) : 3001. [epub] 20190228

Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae)

. 2017 Feb ; 119 (3) : 409-416. [epub] 20161226

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb

. 2016 Sep ; 125 (4) : 683-99. [epub] 20151205

Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants

. 2016 Jun 03 ; 6 () : 27161. [epub] 20160603

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...