全部 标题 作者
关键词 摘要

PLOS ONE  2013 

Epigenetic Differentiation Persists after Male Gametogenesis in Natural Populations of the Perennial Herb Helleborus foetidus (Ranunculaceae)

DOI: 10.1371/journal.pone.0070730

Full-Text   Cite this paper   Add to My Lib


Despite the importance of assessing the stability of epigenetic variation in non-model organisms living in real-world scenarios, no studies have been conducted on the transgenerational persistence of epigenetic structure in wild plant populations. This gap in knowledge is hindering progress in the interpretation of natural epigenetic variation. By applying the methylation-sensitive amplified fragment length polymorphism (MSAP) technique to paired plant-pollen (i.e., sporophyte-male gametophyte) DNA samples, and then comparing methylation patterns and epigenetic population differentiation in sporophytes and their descendant gametophytes, we investigated transgenerational constancy of epigenetic structure in three populations of the perennial herb Helleborus foetidus (Ranunculaceae). Single-locus and multilocus analyses revealed extensive epigenetic differentiation between sporophyte populations. Locus-by-locus comparisons of methylation status in individual sporophytes and descendant gametophytes showed that ~75% of epigenetic markers persisted unchanged through gametogenesis. In spite of some epigenetic reorganization taking place during gametogenesis, multilocus epigenetic differentiation between sporophyte populations was preserved in the subsequent gametophyte stage. In addition to illustrating the efficacy of applying the MSAP technique to paired plant-pollen DNA samples to investigate epigenetic gametic inheritance in wild plants, this paper suggests that epigenetic differentiation between adult plant populations of H. foetidus is likely to persist across generations.


[1]  Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168: 81–91.
[2]  Richards EJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nature Rev Genet 7: 395–401.
[3]  Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Letters 11: 106–115.
[4]  Richards CL, Bossdorf O, Pigliucci M (2010) What role does heritable epigenetic variation play in phenotypic evolution? Bioscience 60: 232–237.
[5]  Kakutani T (2002) Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell Physiol 43: 1106–1111.
[6]  Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Quart Rev Biol 84: 131–176.
[7]  Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. Proc Natl Acad Sci USA 95: 5824–5829.
[8]  Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
[9]  Manning K, Tor M, Poole M, Hong Y, Thompson AJ, et al. (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genet 38: 948–952.
[10]  Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, et al.. (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5: ,e1000530.
[11]  Noyer JL, Causse S, Tomekpe K, Bouet A, Baurens FC (2005) A new image of plantain diversity assessed by SSR, AFLP and MSAP markers. Genetica 124: 61–69.
[12]  Vaughn MW, Tanurdzic M, Lippman Z, Jiang H, Carrasquillo R, et al. (2007) Epigenetic natural variation in Arabidopsis thaliana. PLoS Biology 5: 1617–1629.
[13]  Fang J, Song C, Zheng Y, Qiao Y, Zhang Z, et al. (2008) Variation in cytosine methylation in Clementine mandarin cultivars. J Hort Sci Biotechnol 83: 833–839.
[14]  Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187: 867–876.
[15]  Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, et al. (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5: e10326.
[16]  Paun O, Bateman RM, Fay MF, Hedren M, Civeyrel L, et al. (2010) Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol Biol Evol 27: 2465–2473.
[17]  Richards CL, Schrey AW, Pigliucci M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Letters 15: 1016–1025.
[18]  Herrera CM, Bazaga P (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20: 1675–1688.
[19]  Herrera CM, Bazaga P (2013) Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. Bot J Linn Soc 171: 441–452.
[20]  Richards EJ (2008) Population epigenetics. Curr Opin Genetics Dev 18: 221–226.
[21]  Richards EJ (2011) Natural epigenetic variation in plant species: a view from the field. Curr Opin Plant Biol 14: 204–209.
[22]  Jablonka E, Lamb MJ (1995) Epigenetic inheritance and evolution. Oxford:Oxford University Press. 346 p.
[23]  Jablonka E (2013) Epigenetic inheritance and plasticity: the responsive germline. Progr Biophysics Mol Biol 111: 99–107.
[24]  Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174: 61–70.
[25]  Scoville AG, Barnett LL, Bodbyl-Roels S, Kelly JK, Hileman LC (2011) Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol 191: 251–263.
[26]  Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185: 1108–1118.
[27]  Novero AU, Mabras MB, Esteban HJ (2012) Epigenetic inheritance of spine formation in sago palm (Metroxylon sagu Roettb). Plant Omics J 5: 559–566.
[28]  Becker C, Weigel D (2012) Epigenetic variation: origin and transgenerational inheritance. Curr Opin Plant Biol 15: 562–567.
[29]  Li YD, Shan XH, Liu XM, Hu LJ, Guo WL, et al. (2008) Utility of the methylation-sensitive amplified polymorphism (MSAP) marker for detection of DNA methylation polymorphism and epigenetic population structure in a wild barley species (Hordeum brevisubulatum). Ecol Res 23: 927–930.
[30]  Gao LX, Geng YP, Li B, Chen JK, Yang J (2010) Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ 33: 1820–1827.
[31]  Flatscher R, Frajman B, Sch?nswetter P, Paun O (2012) Environmental heterogeneity and phenotypic divergence: can heritable epigenetic variation aid speciation? Gen Res Int 2012: 9 doi:10.1155/2012/698421.
[32]  Berger F, Twell D (2011) Germline specification and function in plants. Ann Rev Plant Biol 62: 461–484.
[33]  Takeda S, Paszkowski J (2006) DNA methylation and epigenetic inheritance during plant gametogenesis. Chromosoma 115: 27–35.
[34]  Migicovsky Z, Kovalchuk I (2012) Epigenetic modifications during angiosperm gametogenesis. Frontiers Plant Gen Genom 3: 20 doi:10.3389/fpls.2012.00020.
[35]  Gutierrez-Marcos JF, Dickinson HG (2012) Epigenetic reprogramming in plant reproductive lineages. Plant Cell Physiol 53: 817–823.
[36]  Mathew B (1989) Hellebores. St. John's Woking, Surrey: Alpine and Garden Society. 180 p.
[37]  Werner K, Ebel F (1994) Zur Lebensgeschichte der Gattung Helleborus L. (Ranunculaceae). Flora 189: 97–130.
[38]  Guitián J, Medrano M, Herrera CM, Sánchez-Lafuente AM (2003) Variation in the structural gender in the hermaphrodite Helleborus foetidus (Ranunculaceae): within- and among-population patterns. Plant Syst Evol 241: 139–151.
[39]  Herrera CM, Bazaga P (2008) Population-genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth-pollinated violet. Mol Ecol 17: 5378–5390.
[40]  Caballero A, Quesada H, Rolán-Alvarez E (2008) Impact of amplified fragment length polymorphism size homoplasy on the estimation of population genetic diversity and the detection of selective loci. Genetics 179: 539–554.
[41]  Pérez-Figueroa A (2013) msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Mol Ecol Res 13: 522–527.
[42]  R Development Core Team (2010) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: http://www.R-project.org. Accessed 2013 Jun 30.
[43]  Xiong LZ, Xu CG, Maroof MAS, Zhang QF (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genetics 261: 439–446.
[44]  Ashikawa I (2001) Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol 45: 31–39.
[45]  Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.
[46]  Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440–9445.
[47]  Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26: 419–420.
[48]  Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol Ecol 16: 3737–3758.
[49]  Legendre P, Legendre L (1998) Numerical ecology. 2nd edition. Amsterdam:Elsevier. 853 p.
[50]  Venables WN, Ripley BD (2002) Modern applied statistics with S. 4th edition. New York:Springer. 495 p.
[51]  SAS Institute (2006) The GLIMMIX Procedure, June 2006. Cary, NCUSA:SAS Institute. Available: http://support.sas.com/rnd/app/papers/gl?immix.pdf. Accessed 2013 Jun 30.
[52]  Castiglioni P, Ajmone-Marsan P, van Wijk R, Motto M (1999) AFLP markers in a molecular linkage map of maize: codominant scoring and linkage group distribution. Theor Appl Gen 99: 425–431.
[53]  Chagné D, Lalanne C, Madur D, Kumar S, Frigério JM, et al. (2002) A high density genetic map of maritime pine based on AFLPs. Ann Forest Sci 59: 627–636.
[54]  Hartigan JA, Hartigan PM (1985) The dip test of unimodality. Ann Stat 13: 70–84.
[55]  Fraley C, Raftery AE, Murphy TB, Scrucca L (2012) mclust Version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation. Technical Report no. 597. Seattle, WAUSA: Department of Statistics, University of Washington. 57 p.
[56]  Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12: 133–139.
[57]  Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nature Rev Genet 13: 97–109.
[58]  Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442: 1046–1049.
[59]  Crawford RMM (2008) Plants at the margin. Ecological limits and climate change. Cambridge: Cambridge University Press. 478 p.
[60]  Dickinson HG, Grant-Downton R (2009) Bridging the generation gap: flowering plant gametophytes and animal germlines reveal unexpected similarities. Biol Rev 84: 589–615.
[61]  Klekowski EJ (1988) Mutation, developmental selection, and plant evolution. New York: Columbia University Press. 373 p.
[62]  Herrera CM (2009) Multiplicity in unity. Plant subindividual variation and interactions with animals. Chicago: University of Chicago Press. 437 p.
[63]  Echlin P (1972) Ultrastructure and ontogeny of pollen in Helleborus foetidus L. IV. Pollen grain maturation. J Cell Sci 11: 111–129.
[64]  Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472.
[65]  Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev Genet 11: 204–220.
[66]  Janousek B, Matsunaga S, Kejnovsky E, Ziuvova J, Vyskot B (2002) DNA methylation analysis of a male reproductive organ specific gene (MROS1) during pollen development. Genome 45: 930–938.
[67]  Oakeley EJ, Jost JP (1996) Non-symmetrical cytosine methylation in tobacco pollen DNA. Plant Mol Biol 31: 927–930.
[68]  Feil R, Berger F (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genetics 23: 192–199.
[69]  Becker C, Hagmann J, Muller J, Koenig D, Stegle O, et al. (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245–249.
[70]  Zhang YY, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197: 314–322.
[71]  Saze H, Scheid OM, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nature Genet 34: 65–69.


comments powered by Disqus