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Epigenetic variability in plants: Heritability, adaptability, evolutionary significance

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Abstract

DNA methylation is the most stable epigenetic modification with a well studied maintenance mechanism in the mitotically dividing cell generations. The plant DNA is methylated at sites of three types, CG, CHG and CHH. The methylation mechanisms of these sites are different and involve functional activity of various DNA methyltransferases and their accessory factors, that largely define the genome locus specificity of methylation. The genome methylation pattern, DNA methylome, in plants is inheritable not only in the dividing cell generations but also to a considerable extent in generations of the whole plants. A great number of spontaneous epimutations, both natural and experimental ones, are known, that have discernible phenotypic manifestations and are stably inheritable in the plant generations as Mendelian traits. A fundamental distinction of such epimutations from classical mutations is their reversibility. The higher plants epigenome is much more flexible compared with their genome. The single-nucleotide epimutation frequency is hundredfolds higher than the mutation frequency. This variability is probably a main source of the plant phenotypic plasticity, that enables them to adapt to changing environment on the time scales too short for adaptive mutations to occur. A dramatic increase in the plant population epigenetic variability on a practically unchanged genetic context is observed when the essential environmental factors are rapidly changing. Being flexible enough for such adaptive changes, on the other hand, epigenome is stable enough for these adaptive variations to be inheritable between the plant generations. Obviously, the epigenetic variations, that enable plants to adapt to the fast changing environmental factors, serve as material for natural selection and other evolutionary processes on the respective time scales. A still another aspect of evolutionary significance is a capability of epigenetic mechanisms to induce transient bursts of genetic variability by transposon mobilization.

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Abbreviations

DMP:

differentially methylated position

DMR:

differentially methylated DNA region

N-DMPs:

non-differentially methylated position

QTL:

quantitative trait locus

RdDM:

RNA-directed DNA methylation

siRNA:

small interfering RNA

SMP:

single methylation polymorphism

References

  1. Vanyushin, B.F. and Ashapkin, V.V., DNA Methylation in Plants, New York: Nova Sci., 2009.

    Google Scholar 

  2. Law, J.A. and Jacobsen, S.E., Establishing, maintaining and modifying DNA methylation patterns in plants and animals, Nat. Rev. Genet., 2010, vol. 11, pp. 204–220. doi 10.1038/nrg2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Vanyushin, B.F. and Ashapkin, V.V., DNA methylation in higher plants: past, present and future, Biochim. Biophys. Acta, 2011, vol. 1809, pp. 360–368. doi 10.1016/jbbagrm.2011.04.006

    Article  CAS  PubMed  Google Scholar 

  4. Feng, S. and Jacobsen, S.E., Epigenetic modifications in plants: an evolutionary perspective, Curr. Opin. Plant Biol., 2011, vol. 14, pp. 179–186. doi 10.1016/jpbi.2010.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zemach, A., Kim, M.Y., Hsieh, P.-H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, S.L., and Zilberman, D., The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin, Cell, 2013, vol. 153, pp. 193–205. doi 10.1016/jcell.2013.02.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., Patel, D.J., and Jacobsen, S.E., Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis, Nat. Struct. Mol. Biol., 2014, vol. 21, pp. 64–72. doi 10.1038/nsmb.2735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cubas, P., Vincent, C., and Coen, E., An epigenetic mutation responsible for natural variation in floral symmetry, Nature, 1999, vol. 401, pp. 157–161.

    Article  CAS  PubMed  Google Scholar 

  8. Jacobsen, S.E. and Meyerowitz, E.M., Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis, Science, 1997, vol. 277, pp. 1100–1103.

    Article  CAS  PubMed  Google Scholar 

  9. Miura, K., Agetsuma, M., Kitano, H., Yoshimura, A., Matsuoka, M., Jacobsen, S.E., and Ashikari, M., A metastable DWARF1 epigenetic mutant affecting plant stature in rice, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 11218–11223. doi 10.1073/pnas.090194210610.1073/pnas.0901942106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., Giovannoni, J.J., and Seymour, G.B., A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening, Nat. Genet., 2006, vol. 38, pp. 948–952. doi 10.1038/ng1841

    Article  CAS  PubMed  Google Scholar 

  11. Kakutani, T., Jeddeloh, J.A., and Richards, E.J., Characterization of an Arabidopsis thaliana DNA hypomethylation mutant, Nucleic Acids Res., 1995, vol. 23, pp. 130–137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J., and Dellaporta, S.L., Demethylation-induced developmental pleiotropy in Arabidopsis, Science, 1996, vol. 273, pp. 654–657. doi 10.1126/science.273.5275.654

    Article  CAS  PubMed  Google Scholar 

  13. Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R., Jeddeloh, J.A., Riddle, N.C., Verbsky, M.L., and Richards, E.J., Arabidopsis MET1 cytosine methyltransferase mutants, Genetics, 2003, vol. 163, pp. 1109–1122.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Akimoto, K., Katakami, H., Kim, H.J., Ogawa, E., Sano, C.M., Wada, Y., and Sano, H., Epigenetic inheritance in rice plants, Ann. Bot., 2007, vol. 100, pp. 205–217. doi 10.1093/aob/mcm110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Teixeira, F.K., Heredia, F., Sarazin, A., Roudier, F., Boccara, M., Ciaudo, C., Cruaud, C., Poulain, J., Berdasco, M., Fraga, M.F., Voinnet, O., Wincker, P., Esteller, M., and Colot, V., A role for RNA in the selective correction of DNA methylation defects, Science, 2009, vol. 323, pp. 1600–1604. doi 10.1126/science.1165313

    Article  CAS  PubMed  Google Scholar 

  16. Fujimoto, R., Sasaki, T., Kudoh, H., Taylor, J.M., Kakutani, T., and Dennis, E.S., Epigenetic variation in the FWA gene within the genus Arabidopsis, Plant J., 2011, vol. 66, pp. 831–843. doi 10.1111/j.1365- 313X.2011.04549x

    Article  CAS  PubMed  Google Scholar 

  17. Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L., and Kakutani, T., One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation, Science, 2004, vol. 303, pp. 521–523. doi 10.1126/science. 1089835

    Article  CAS  PubMed  Google Scholar 

  18. Shiba, H. and Takayama, S., Epigenetic regulation of monoallelic gene expression, Dev. Growth Differ., 2012, vol. 54, pp. 120–128. doi 10.1111/j.1440-169X.2011.01317x

    Article  CAS  PubMed  Google Scholar 

  19. Köhler, C. and Kradolfer, D., Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants, Biochim. Biophys. Acta, 2011, vol. 1809, pp. 438–443. doi 10.1016/jbbagrm.2011.04.004

    Article  PubMed  Google Scholar 

  20. Xiao, W., Gehring, M., Choi, Y., Margossian, L., Pu, H., Harada, J.J., Goldberg, R.B., Pennell, R.I., and Fischer, R.L., Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase, Dev. Cell, 2003, vol. 5, pp. 891–901.

    Article  CAS  PubMed  Google Scholar 

  21. Lauria, M., Rupe, M., Guo, M., Kranz, E., Pirona, R., Viotti, A., and Lund, G., Extensive maternal DNA hypomethylation in the endosperm of Zea mays, Plant Cell, 2004, vol. 16, pp. 510–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bushell, C., Spielman, M., and Scott, R.J., The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species, Plant Cell, 2003, vol. 15, pp. 1430–1442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dyachenko, O.V., Zakharchenko, N.S., Shevchuk, T.V., Bohnert, H.J., Cushman, J.S., and Buryanov, Ya.I., Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress, Biochemistry (Moscow), 2006, vol. 71, pp. 461–465.

    Article  CAS  Google Scholar 

  24. Verhoeven, K.J.F., Jansen, J.J., van Dijk, P.J., and Biere, A., Stress-induced DNA methylation changes and their heritability in asexual dandelions, New Phytol., 2010, vol. 185, pp. 1108–1118. doi 10.1111/j.1469-8137.2009.03121x

    Article  CAS  PubMed  Google Scholar 

  25. Lira-Medeiros, C.F., Parisod, C., Fernandes, R.A., Mata, C.S., Cardoso, M.A., and Ferreira, P.C.G., Epigenetic variation in mangrove plants occurring in contrasting natural environment, PLoS One, 2010, vol. 5: e10326. doi 10.1371/journalpone.0010326

    Article  PubMed  PubMed Central  Google Scholar 

  26. Richards, C.L., Schrey, A.W., and Pigliucci, M., Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation, Ecol. Lett., 2012, vol. 15, pp. 1016–1025. doi 10.1111/j.1461-0248.2012.01824x

    Article  PubMed  Google Scholar 

  27. Shen, X., de Jonge, J., Forsberg, S.K.G., Pettersson, M.E., Sheng, Z., Hennig, L., and Carlborg, O., Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality, PLoS Genet., 2014, vol. 10, pp. e1004842. doi 10.1371/journalpgen.1004842

    Article  Google Scholar 

  28. Dubin, M.J., Zhang, P., Meng, D., Remigereau, M.-S., Osborne, E.J., Casale, F.P., Drewe, P., Kahles, A., Jean, G., Vilhjalmsson, B., Jagoda, J., Irez, S., Voronin, V., Song, Q., Long, Q., et al., DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation, eLife, 2015, vol. 4, pp. e05255. doi 10.7554/eLife.05255

    Article  Google Scholar 

  29. West, P.T., Li, Q., Ji, L., Eichten, S.R., Song, J., Vaughn, M.W., Schmitz, R.J., and Springer, N.M., Genomic distribution of H3K9me2 and DNA methylation in a maize genome, PLoS One, 2014, vol. 9, pp. e105267. doi 10.1371/journalpone.0105267

    Article  Google Scholar 

  30. Miura, A., Yonebayashi, S., Watanabe, K., Toyama, T., Shimada, H., and Kakutani, T., Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis, Nature, 2001, vol. 411, pp. 212–214.

    Article  CAS  PubMed  Google Scholar 

  31. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M., and Jacobsen, S.E., Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning, Nature, 2008, vol. 452, pp. 215–219. doi 10.1038/nature06745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lister, R., O’Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H., and Ecker, J.R., Highly integrated single-base resolution maps of the epigenome in Arabidopsis, Cell, 2008, vol. 133, pp. 523–536. doi 10.1016/jcell.2008.03.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ossowski, S., Schneeberger, K., Lucas-Lledo, J.I., Warthmann, N., Clark, R.M., Shaw, R.G., Weigel, D., and Lynch, M., The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana, Science, 2010, vol. 327, pp. 92–94. doi 10.1126/science. 1180677

    Article  CAS  PubMed  Google Scholar 

  34. Schmitz, R.J., Schultz, M.D., Lewsey, M.G., O’Malley, R.C., Urich, M.A., Libiger, O., Schork, N.J., and Ecker, J.R., Transgenerational epigenetic instability is a source of novel methylation variants, Science, 2011, vol. 334, pp. 369–373. doi 10.1126/science.1212959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Becker, C., Hagmann, J., Muller, J., Koenig, D., Stegle, O., Borgwardt, K., and Weigel, D., Spontaneous epigenetic variation in the Arabidopsis thaliana methylome, Nature, 2011, vol. 480, pp. 245–249. doi 10.1038/nature10555

    Article  CAS  PubMed  Google Scholar 

  36. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D., and Sundaresan, V., Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis, Development, 2005, vol. 132, pp. 603–614. doi 10.1242/dev.01595

    Article  CAS  PubMed  Google Scholar 

  37. Cao, J., Schneeberger, K., Ossowski, S., Günther, T., Bender, S., Fitz, J., Koenig, D., Lanz, C., Stegle, O., Lippert, C., Wang, X., Ott, F., Müller, J., Alonso-Blanco, C., Borgwardt, K., et al., Whole-genome sequencing of multiple Arabidopsis thaliana populations, Nat. Genet., 2011, vol. 43, pp. 956–963. doi 10.1038/ng.911

    Article  CAS  PubMed  Google Scholar 

  38. Schmitz, R.J. and Ecker, J.R., Epigenetic and epigenomic variation in Arabidopsis thaliana, Trends Plant Sci., 2012, vol. 17, pp. 149–154. doi 10.1016/jtplants.2012.01.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu, J., He, Y., Amasino, R., and Chen, X., siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis, Genes Dev., 2004, vol. 18, pp. 2873–2878. doi 10.1101/gad.1217304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., and Paszkowski, J., An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress, Nature, 2011, vol. 472, pp. 115–119. doi 10.1038/nature09861

    Article  CAS  PubMed  Google Scholar 

  41. Bender, J. and Fink, G.R., Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis, Cell, 1995, vol. 83, pp. 725–734.

    Article  CAS  PubMed  Google Scholar 

  42. Schmitz, R.J., Schultz, M.D., Urich, M., Nery, J.R., Pelizzola, M., Libiger, O., Alix, A., McCosh, R.B., Chen, H., Schork, N.J., and Ecker, J.R., Patterns of population epigenomic diversity, Nature, 2013, vol. 495, pp. 193–198. doi 10.1038/nature11968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Aravin, A.A., Sachidanandam, R., Bourchis, D., Schaefer, C., Pezic, D., Toth, K.F., Bestor, T., and Hannon, G.J., A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice, Mol. Cell, 2008, vol. 31, pp. 785–799. doi 10.1016/jmolcel.2008.09.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cortijo, S., Wardenaar, R., Colomé-Tatché, M., Gilly, A., Etcheverry, M., Labadie, K., Caillieux, E., Hospital, F., Aury, J.-M., Wincker, P., Roudier, F., Jansen, R.C., Colot, V., and Johannes, F., Mapping the epigenetic basis of complex traits, Science, 2014, vol. 343, pp. 1145–1148. doi 10.1126/science.1248127

    Article  CAS  PubMed  Google Scholar 

  45. Eichten, S.R., Schmitz, R.J., and Springer, N.M., Epigenetics: beyond chromatin modifications and complex genetic regulation, Plant Physiol., 2014, vol. 165, pp. 933–947. doi 10.1104/pp.113.234211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 119991, Russia

    V. V. Ashapkin, L. I. Kutueva & B. F. Vanyushin

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  1. V. V. Ashapkin
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  2. L. I. Kutueva
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  3. B. F. Vanyushin
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Correspondence to V. V. Ashapkin.

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Published in Russian in Fiziologiya Rastenii, 2016, Vol. 63, No. 2, pp. 191–204.

The article was translated by the authors.

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Ashapkin, V.V., Kutueva, L.I. & Vanyushin, B.F. Epigenetic variability in plants: Heritability, adaptability, evolutionary significance. Russ J Plant Physiol 63, 181–192 (2016). https://doi.org/10.1134/S1021443716020059

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