Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae)
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
PubMed
28025291
PubMed Central
PMC5314647
DOI
10.1093/aob/mcw229
PII: mcw229
Knihovny.cz E-zdroje
- Klíčová slova
- DNA base composition, DNA content, Droseraceae, GC content, carnivorous plants, flow cytometry, genome size evolution, holocentric chromosomes, holokinetic chromosomes,
- MeSH
- biologická evoluce * MeSH
- chromozomy rostlin genetika MeSH
- Droseraceae genetika MeSH
- fylogeneze MeSH
- genetická variace genetika MeSH
- genom rostlinný genetika MeSH
- masožravci MeSH
- zastoupení bazí genetika MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND AND AIMS: Studies in the carnivorous family Lentibulariaceae in the last years resulted in the discovery of the smallest plant genomes and an unusual pattern of genomic GC content evolution. However, scarcity of genomic data in other carnivorous clades still prevents a generalization of the observed patterns. Here the aim was to fill this gap by mapping genome evolution in the second largest carnivorous family, Droseraceae, where this evolution may be affected by chromosomal holokinetism in Drosera METHODS: The genome size and genomic GC content of 71 Droseraceae species were measured by flow cytometry. A dated phylogeny was constructed, and the evolution of both genomic parameters and their relationship to species climatic niches were tested using phylogeny-based statistics. KEY RESULTS: The 2C genome size of Droseraceae varied between 488 and 10 927 Mbp, and the GC content ranged between 37·1 and 44·7 %. The genome sizes and genomic GC content of carnivorous and holocentric species did not differ from those of their non-carnivorous and monocentric relatives. The genomic GC content positively correlated with genome size and annual temperature fluctuations. The genome size and chromosome numbers were inversely correlated in the Australian clade of Drosera CONCLUSIONS: Our results indicate that neither carnivory (nutrient scarcity) nor the holokinetism have a prominent effect on size and DNA base composition of Droseraceae genomes. However, the holokinetic drive seems to affect karyotype evolution in one of the major clades of Drosera Our survey confirmed that the evolution of GC content is tightly connected with the evolution of genome size and also with environmental conditions.
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Bennett MD. 1972. Nuclear DNA content and minimum generation time in herbaceous plants. Proceedings of the Royal Society B: Biological Sciences 181: 109–135. PubMed
Bennett MD, Leitch IJ. 2012. Angiosperm DNA C-values database (release 8·0, December 2012). http://data.kew.org/cvalues/ (last accessed 17 January 2016).
Biro JC. 2008. Correlation between nucleotide composition and folding energy of coding sequences with special attention to wobble bases. Theoretical Biology and Medical Modelling 5: 14. PubMed PMC
Brummitt RK. 2001. World geographical scheme for recording plant distributions, 2nd edm Pittsburgh: Hunt Institute for Botanical Documentation, Carnegie-Mellon University.
Bureš P, Zedek F. 2014. Holokinetic drive: centromere drive in chromosomes without centromeres. Evolution 68: 2412–2420. PubMed
Bureš P, Šmarda P, Hralová I, et al. 2007. Correlation between GC content and genome size in plants. Cytometry A 71A: 764.
Bureš P, Zedek F, Marková M. 2013. Holocentric chromosomes In: Wendel J, Greilhuber J, Doležel J, Leitch IJ, eds. Plant genome diversity. Vol. 2. Physical structure of plant genomes. Heidelberg: Springer, 187–208.
Chung KS, Hipp AL, Roalson EH. 2012. Chromosome number evolves independently of genome size in a clade with nonlocalized centromeres (Carex: Cyperaceae). Evolution 66: 2708–2722. PubMed
Cuacos M, H Franklin FC, Heckmann S. 2015. Atypical centromeres in plants – what they can tell us. Frontiers in Plant Sciences 6: 913. PubMed PMC
Demidov D, Schubert V, Kumke K, et al.. 2014. Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenetics and Genome Research 143: 150–156. PubMed
Escudero M, Hipp AL., Hansen TF, Voje KL., Luceño M. 2012. Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). New Phytologist 195: 237–247. PubMed
Escudero M, Maguilla E, Loureiro J, Castro M, Castro S, Luceño M. 2015. Genome size stability despite high chromosome number variation in Carex gr. laevigata. American Journal of Botany 102: 233–238. PubMed
Fleischmann A, Michael TP, Rivadavia F, et al.. 2014. Evolution of genome size and chromosome numbers in the carnivorous plant genus Genlisea (Lentibulariaceae). Annals of Botany 114: 1651–1663. PubMed PMC
Foerstner KU, von Mering C, Hooper SD, Bork P. 2005. Environments shape the nucleotide composition of genomes. EMBO Reports 6: 1208–1213. PubMed PMC
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JE. 1984. Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. American Naturalist 124: 479–497.
Gonella PM, Rivadavia F, Fleischmann A. 2015. Drosera magnifica (Droseraceae): the largest New World sundew, discovered on Facebook. Phytotaxa 220: 257–267.
Govaerts R, Cheek M. 2014. World Checklist of Droseraceae Facilitated by the Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp/ (last accessed 20 May 2015).
Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott W. 2006. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biology 8: 770–777. PubMed
Greilhuber J, Doležel J, Lysák MA, Bennet MD. 2005. The origin, evolution and proposed stabilization of the terms ‘Genome Size’ and ‘C-Value’ to describe nuclear DNA contents. Annals of Botany 95: 255–260. PubMed PMC
Harmon L, Weir J, Brock C, et al. 2015. Geiger:analysis of evolutionary diversification. Version 2.0.6 https://cran.r-project.org/web/packages/geiger/geiger.pdf (last accessed 25 January 2016).
Heckmann S, Houben A. 2013. Holokinetic centromeres In: Jiang J, Birchler JA, eds. Plant centromere biology. Oxford: Wiley-Blackwell, 83–94.
Heubl G, Bringmann G, Meimberg H. 2006. Molecular phylogeny and character evolution of carnivorous plant families in Caryophyllales – revisited. Plant Biology 8: 821–830. PubMed
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965–1978.
Ibarra-Laclette E, Albert VA, Herrera-Estrella A, Herrera-Estrella L. 2011a. Is GC bias in the nuclear genome of the carnivorous plant Utricularia driven by ROS-based mutation and biased gene conversion? Plant Signaling and Behavior 6: 1631–1634. PubMed PMC
Ibarra-Laclette E, Albert VA, Perez-Torres CA, et al. 2011b. Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome. BMC Plant Biology 11: 101. PubMed PMC
Ibarra-Laclette E, Lyons E, Hernández-Guzmán G, et al.. 2013. Architecture and evolution of a minute plant genome. Nature 498: 94–98. PubMed PMC
International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. Nature 436: 793–800. PubMed
Jensen MK, Vogt JK, Bressendorff S, et al.. 2015. Transcriptome and genome size analysis of the venus flytrap. PLoS One 10: e0123887. PubMed PMC
Jobson RW, Albert VA. 2002. Molecular rates parallel diversification contrasts between carnivorous plant sister lineages. Cladistics 18: 127–136. PubMed
Kondo K, Nontachaiyapoom S. 2008. An evidence on diffused centromeres in Drosera chromosomes provided by scanning electron microscopy. Chromosome Botany 3: 79–81.
Leitch AR, Leitch IJ. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481–483. PubMed
Leushkin EV, Sutormin RA, Nabieva ER, Penin AA, Kondrashov AS, Logacheva MD. 2013. The miniature genome of a carnivorous plant Genlisea aurea contains a low number of genes and short non-coding sequences. BMC Genomics 14: 476. PubMed PMC
Lipnerová I, Bureš P, Horová L, Šmarda P. 2013. Evolution of genome size in Carex (Cyperaceae) in relation to chromosome number and genomic base composition. Annals of Botany 111: 79–94. PubMed PMC
Lukhtanov VA, Shapoval NA, Anokhin BA, Saifitdinova AF, Kuznetsova VG. 2015. Homoploid hybrid speciation and genome evolution via chromosome sorting. Proceedings of the Royal Society B: Biological Sciences 282: 20150157. PubMed PMC
Mann S, Phoebe-Chen YP. 2010. Bacterial genomic G + C composition-eliciting environmental adaptation. Genomics 95: 7–15. PubMed
McPherson S. 2008. Glistening carnivores the sticky-leaved insect-eating plants. Poole, UK: Redfern Natural History Productions.
McPherson S. 2010. Carnivorous plants and their habitats, vol. 2. Poole, UK: Redfern Natural History Productions.
Musto H, Naya H, Zavala A, et al.. 2006. Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochemical and Biophysical Research Communications 347: 1–3. PubMed
Nishikawa K, Furuta Y, Ishitobi K. 1984. Chromosomal evolution in genus Carex as viewed from nuclear-DNA content, with special reference to its aneuploidy. Japanese Journal of Genetics 59: 465–472.
Nishio Y, Nakamura Y, Kawarabayasi Y, et al. 2003. Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Research 13: 1572–1579. PubMed PMC
Orme D, Freckleton R, Thomas G, et al. 2012. Caper: comparative analyses of phylogenetics and evolution in R. Version 0.5 http://cran.r-project.org/web/packages/caper/caper.pdf (last accessed 25 April 2013).
Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. PubMed
R Core Team . 2013. R: a language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/ (last accessed 25 April 2013).
Revell LJ. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223.
Rivadavia F, de Miranda VFO, Hoogenstrijd G, Pinheiro F, Heubl G, Fleichmann A. 2012. Is Drosera meristocaulis a pygmy sundew? Evidence of a long-distance dispersal between Western Australia and northern South America. Annals of Botany 110: 11–21. PubMed PMC
Roalson E, McCubbin AG, Whitkus R. 2007. Chromosome evolution in Cyperales In: Columbus JT, Friar EA, Porter JM, Prince LM, Simpson MG, eds. Monocots: comparative biology and evolution of Poales. Claremont, CA: Allen, 62–71.
Rothfels K, Heimburg M. 1968. Chromosome size and DNA values in sundews (Droseraceae). Chromosoma 25: 96–103.
Sheikh SA, Kondo K, Hoshi Y. 1995. Study of diffused centromeric nature of Drosera chromosomes. Cytologia 60: 43–47.
Shirakawa J, Hoshi Y, Kondo K. 2011a. Chromosome differentiation and genome organization in carnivorous plant family Droseraceae. Chromosome Botany 6: 111–119.
Shirakawa J, Nagano K, Hoshi Y. 2011b. A chromosome study of two centromere differentiating Drosera species, D. arcturi and D. regia. Caryologia 64: 453–563.
Šíchová J., Ohno M, Dincă V, Watanabe M, Sahara K, Marec F. 2016. Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis. Biological Journal of the Linnean Society 118: 457–451.
Šmarda P, Bureš P. 2012. The variation of base composition in plant genomes In: Wendel JF, Greilhuber J, Doležel J, Leitch IJ, eds. Plant genome diversity, vol. 1 Vienna: Springer, 209–235.
Šmarda P, Bureš P, Horová L, Foggi B, Rossi G. 2008. Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction. Annals of Botany 101: 421–433. PubMed PMC
Šmarda P, Bureš P, Horová L, et al. 2014. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proceedings of the National Academy of Sciences, USA 111: E4096–E4102. PubMed PMC
Sterner RW, Elser JJ. 2002. Ecological stoichiometry. The biology of elements from molecules to biosphere. Princeston and Oxford: Princeston University Press.
Veleba A, Bureš P, Adamec L, Šmarda P, Lipnerová I, Horová I. 2014. Genome size and genomic GC content evolution in the miniature genome-sized family Lentibulariaceae. New Phytologist 203: 22–28. PubMed
Veselý P, Bureš P, Šmarda P, Pavlíček T. 2012. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany 109: 65–75. PubMed PMC
Vu GTH, Schmutzer T, Bull F, et al.. 2015. Comparative genome analysis reveals divergent genome size evolution in a carnivorous plant genus. Plant Genome 8: 3. doi:10.3835/plantgenome2015.04.0021. PubMed
Wendel J, Greilhuber J, Doležel J, Leitch IJ. 2013. Plant genome diversity. Vol. 2. Physical structure of plant genomes. Heidelberg: Springer.
Záveská Drábková L, Vlček C. 2010. Molecular phylogeny of the genus Luzula DC. (Juncaceae, Monocotyledones) based on plastome and nuclear ribosomal regions: a case of incongruence, incomplete lineage sorting and hybridisation. Molecular Phylogenetics and Evolution 57: 536–551. PubMed
Zedek F, Bureš P. 2016. Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Annals of Botany (in press). PubMed PMC
Zedek F, Šmerda J, Šmarda P, Bureš P. 2010. Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biology 10: 265. PubMed PMC
Zedek F, Veselý P, Horová L, Bureš P. 2016. Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants. Scientific Reports 6: 27161. doi: 10.1038/srep27161. PubMed PMC
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