Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana

. 2018 Sep ; 121 (3) : 257-265. [epub] 20180606

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29875373
Odkazy

PubMed 29875373
PubMed Central PMC6082859
DOI 10.1038/s41437-018-0095-9
PII: 10.1038/s41437-018-0095-9
Knihovny.cz E-zdroje

Increasing evidence for epigenetic variation within and among natural plant populations has led to much speculation about its role in the evolution of plant phenotypes. However, we still have a very limited understanding of the evolutionary potential of epigenetic variation, in particular in comparison to DNA sequence-based variation. To address this question, we compared the magnitudes of heritable phenotypic variation in epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana-lines that mainly differ in DNA methylation but only very little in DNA sequence-with other types of A. thaliana lines that differ strongly also in DNA sequence. We grew subsets of two epiRIL populations with subsets of two genetic RIL populations, of natural ecotype collections, and of lines from a natural population in a common environment and assessed their heritable variation in growth, phenology, and fitness. Among-line phenotypic variation and broad-sense heritabilities tended to be largest in natural ecotypes, but for some traits the variation among epiRILs was comparable to that among RILs and natural ecotypes. Within-line phenotypic variation was generally similar in epiRILs, RILs, and ecotypes. Provided that phenotypic variation in epiRILs is mainly caused by epigenetic differences, whereas in RILs and natural lines it is largely driven by sequence variation, our results indicate that epigenetic variation has the potential to create phenotypic variation that is stable and substantial, and thus of evolutionary significance.

Zobrazit více v PubMed

Alonso-Blanco C, Koornneef M. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci. 2000;5:22–29. doi: 10.1016/S1360-1385(99)01510-1. PubMed DOI

Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011;480:245–249. doi: 10.1038/nature10555. PubMed DOI

Bird A. Perceptions of epigenetics. Nature. 2007;447:396–398. doi: 10.1038/nature05913. PubMed DOI

Bossdorf O, Richards CL, Pigliucci M. Epigenetics for ecologists. Ecol Lett. 2008;11:106–115. PubMed

Brachi B, Villoutreix R, Faure N, Hautekeete N, Piquot Y, Pauwels M, et al. Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana. Mol Ecol. 2013;22:4222–4240. doi: 10.1111/mec.12396. PubMed DOI

Colome-Tatche M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, et al. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci USA. 2012;109:16240–16245. doi: 10.1073/pnas.1212955109. PubMed DOI PMC

Conner JK, Franks R, Stewart C. Expression of additive genetic variances and covariances for wild radish floral traits: Comparison between field and greenhouse environments. Evolution. 2003;57:487–495. doi: 10.1111/j.0014-3820.2003.tb01540.x. PubMed DOI

Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K, et al. Mapping the epigenetic basis of complex traits. Science. 2014;343:1145–1148. doi: 10.1126/science.1248127. PubMed DOI

Cubas P, Vincent C, Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 1999;401:157–161. doi: 10.1038/43657. PubMed DOI

Dubin MJ, Zhang P, Meng D, Remigereau MS, Osborne EJ, Casale FP, et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife. 2015;4:e05255. doi: 10.7554/eLife.05255. PubMed DOI PMC

Falconer DS, Mackay TFC. Introduction to quantitative genetics. New York, NY, USA: Longman; 1996.

Finnegan EJ, Kovac KA. Plant DNA methyltransferases. Plant Mol Biol. 2000;43:189–201. doi: 10.1023/A:1006427226972. PubMed DOI

Fisher RA. The genetical theory of natural selection. Oxford, UK: Oxford University Press; 1930.

Futuyma DJ. Evolution. Sunderland, Massachusetts, USA: Sinauer associates, Inc; 2013.

Hansen TF, Pelabon C, Houle D. Heritability is not evolvability. Evol Biol. 2011;38:258–277. doi: 10.1007/s11692-011-9127-6. DOI

Herrera CM, Bazaga P. Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol. 2011;20:1675–1688. doi: 10.1111/j.1365-294X.2011.05026.x. PubMed DOI

Johannes F, Colot V, Jansen RC. OPINION Epigenome dynamics: a quantitative genetics perspective. Nat Rev Genet. 2008;9:883–890. doi: 10.1038/nrg2467. PubMed DOI

Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009;5:e1000530. doi: 10.1371/journal.pgen.1000530. PubMed DOI PMC

Kakutani T, Jeddeloh JA, Richards EJ. Characterization of an Arabidopsis thaliana DNA hypomethylation mutant. Nucleic Acids Res. 1995;23:130–137. doi: 10.1093/nar/23.1.130. PubMed DOI PMC

Kawakatsu T, Huang SSC, Jupe F, Sasaki E, Schmitz RJ, Urich MA, et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell. 2016;166:492–505. doi: 10.1016/j.cell.2016.06.044. PubMed DOI PMC

Kooke R, Johannes F, Wardenaar R, Becker F, Etcheverry M, Colot V, et al. Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell. 2015;27:337–348. doi: 10.1105/tpc.114.133025. PubMed DOI PMC

Koornneef M, Alonso-Blanco C, Vreugdenhil D. Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol. 2004;55:141–172. doi: 10.1146/annurev.arplant.55.031903.141605. PubMed DOI

Latzel V, Allan E, Silveira AB, Colot V, Fischer M, Bossdorf O. Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun. 2013;4:2875. doi: 10.1038/ncomms3875. PubMed DOI

Latzel V, Zhang Y, Moritz KK, Fischer M, Bossdorf O. Epigenetic variation in plant responses to defence hormones. Ann Bot. 2012;110:1423–1428. doi: 10.1093/aob/mcs088. PubMed DOI PMC

Lister C, Dean C. Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J. 1993;4:745–750. doi: 10.1046/j.1365-313X.1993.04040745.x. PubMed DOI

Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;133:523–536. doi: 10.1016/j.cell.2008.03.029. PubMed DOI PMC

Loudet O, Chaillou S, Camilleri C, Bouchez D, Daniel-Vedele F. Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor Appl Genet. 2002;104:1173–1184. doi: 10.1007/s00122-001-0825-9. PubMed DOI

Morgado L, Preite V, Oplaat C, Anava S, Ferreira de Carvalho J, Rechavi O, et al. Small RNAs reflect grandparental environments in apomictic dandelion. Mol Biol Evol. 2017;34:2035–2040. doi: 10.1093/molbev/msx150. PubMed DOI PMC

Ossowski S, Schneeberger K, Lucas-Lledo JI, Warthmann N, Clark RM, Shaw RG, et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science. 2010;327:92–94. doi: 10.1126/science.1180677. PubMed DOI PMC

Pigliucci M. Ecology and evolutionary biology of Arabidopsis. Arab Book / Am Soc Plant Biol. 2002;1:e0003. doi: 10.1199/tab.0003. PubMed DOI PMC

Pigliucci M, Marlow ET. Differentiation for flowering time and phenotypic integration in Arabidopsis thaliana in response to season length and vernalization. Oecologia. 2001;127:501–508. doi: 10.1007/s004420000613. PubMed DOI

Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2013). nlme: Linear and nonlinear mixed effects models. R package version 3.1-113, https://CRAN.R-project.org/package=nlme

Platt A, Horton M, Huang YS, Li Y, Anastasio AE, Mulyati NW, et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet. 2010;6:e1000843. doi: 10.1371/journal.pgen.1000843. PubMed DOI PMC

R Core Team (2013) R Foundation for Statistical Computing: Vienna, Austria.

Reinders J, Paszkowski J. Unlocking the Arabidopsis epigenome. Epigenetics. 2009;4:557–563. doi: 10.4161/epi.4.8.10347. PubMed DOI

Reinders J, Wulff BBH, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009;23:939–950. doi: 10.1101/gad.524609. PubMed DOI PMC

Richards CL, Alonso C, Becker C, Bossdorf O, Bucher E, Colome-Tatche M, et al. Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecol Lett. 2017;20:1576–1590. doi: 10.1111/ele.12858. PubMed DOI

Richards EJ. OPINION Inherited epigenetic variation - revisiting soft inheritance. Nat Rev Genet. 2006;7:395–401. doi: 10.1038/nrg1834. PubMed DOI

Roux F, Colome-Tatche M, Edelist C, Wardenaar R, Guerche P, Hospital F, et al. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics. 2011;188:1015–1017. doi: 10.1534/genetics.111.128744. PubMed DOI PMC

Saze H, Scheid OM, Paszkowski J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet. 2003;34:65–69. doi: 10.1038/ng1138. PubMed DOI

Schmitz RJ, He Y, Valdes-Lopez O, Khan SM, Joshi T, Urich MA, et al. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 2013;23:1663–1674. doi: 10.1101/gr.152538.112. PubMed DOI PMC

Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011;334:369–373. doi: 10.1126/science.1212959. PubMed DOI PMC

Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, et al. Patterns of population epigenomic diversity. Nature. 2013;495:193–198. doi: 10.1038/nature11968. PubMed DOI PMC

Simons AM, Roff DA. The effect of environmental variability on the heritabilities of traits of a field cricket. Evolution. 1994;48:1637–1649. doi: 10.1111/j.1558-5646.1994.tb02201.x. PubMed DOI

Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, et al. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA. 2004;101:4712–4717. doi: 10.1073/pnas.0306401101. PubMed DOI PMC

Stroud H, Greenberg MVC, Feng SH, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013;152:352–364. doi: 10.1016/j.cell.2012.10.054. PubMed DOI PMC

Ungerer MC, Halldorsdottir SS, Modliszewski JL, Mackay TFC, Purugganan MD. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics. 2002;160:1133–1151. PubMed PMC

van der Graaf A, Wardenaar R, Neumann DA, Taudt A, Shaw RG, Jansen RC, et al. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc Natl Acad Sci USA. 2015;112:6676–6681. doi: 10.1073/pnas.1424254112. PubMed DOI PMC

Vidalis A, Živković D, Wardenaar R, Roquis D, Tellier A, Johannes F. Methylome evolution in plants. Genome Biol. 2016;17:264. doi: 10.1186/s13059-016-1127-5. PubMed DOI PMC

Vongs A, Kakutani T, Martienssen RA, Richards EJ. Arabidopsis thaliana DNA methylation mutants. Science. 1993;260:1926–1928. doi: 10.1126/science.8316832. PubMed DOI

Wilschut RA, Oplaat C, Snoek LB, Kirschner J, Verhoeven KJF. Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage. Mol Ecol. 2016;25:1759–1768. doi: 10.1111/mec.13502. PubMed DOI

Wolfe MD, Tonsor SJ. Adaptation to spring heat and drought in northeastern Spanish Arabidopsis thaliana. New Phytol. 2014;201:323–334. doi: 10.1111/nph.12485. PubMed DOI

Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;153:193–205. doi: 10.1016/j.cell.2013.02.033. PubMed DOI PMC

Zhang YY, Fischer M, Colot V, Bossdorf O. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 2013;197:314–322. doi: 10.1111/nph.12010. PubMed DOI

Zobrazit více v PubMed

Dryad
10.5061/dryad.b7bq47d

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...