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RESEARCH

Extending the Modern Synthesis

The Modern Synthesis fused Mendelian genetics and Darwinian evolution to provide a unified theory of evolution [1]. Heritable, genetic changes that contribute to phenotypic differences between individuals of a population are the foundations of the Modern Synthesis. However, epigenetics, the molecular mechanism of heritable gene expression changes that cannot be attributed to changes in DNA sequence information, potentially offers an alternative path for evolution [2]. Unlike epigenetics, which implies the mechanism, the epigenome, which includes all post-translational modifications and other chromatin features associated with regulatory elements in the genome, potentially provides the substrate for evolution [2]. Indeed, the generation of epialleles through natural and induced sources has given rise to novel phenotypic variation, ranging from altered disease resistance, variation in biomass, oil yield, and flower morphology within a population (Fig. 1) [3–6]. I am interested in how epigenetics and the epigenome fits within the Modern Synthesis.

peloric.png

Figure 1. An epigenetic mutation responsible for natural variation in floral symmetry in Linaria vulgaris (toadflax) [3]. The Lcyc gene is methylated and transcriptionally silent in the peloric mutant. This epiallele co-segregates with the mutant phenotype. Figure modified from [3].

The evolutionary origins and function of epigenomic variation

Sparse sampling of DNA and histone modifications, and taxonomic groups hinder our understanding of the evolutionary origins and function of epigenomic variation. Furthermore, explanations for the observed patterns of 5-methylcytosine (5mC) – the most well studied type of epigenomic variation – and its functional importance, remain largely unknown [7–11] (Fig. 2). It is only through strengthening our understanding of the evolution of genetic mechanisms that establish and maintain DNA and histone modifications, genome evolution, life history, and modification crosstalk can we develop a comprehensive theory for the origins and function of epigenomic variation. I am interested in pairing comparative methods with functional genetics to test hypotheses for the evolutionary origins and function of epigenomic variation.

cg_methylation.plants.bw.landscape_10062

Figure 2. Epigenomic variation across Chlorophyta and within Arabidopsis thaliana.

Epigenome editing for crop improvement

The epigenome harnesses the potential for crop improvement without perturbing established genetic associations. Work in the model plant Arabidopsis thaliana has radically changed our perception of the epigenomic contributions to complex phenotypic traits [11]. Furthermore, the development of promising new methodologies for engineering 5mC states in a site-specific manner in plant genomes make testing the effect of epialleles on phenotypic traits possible [12]. A limiting step in epigenome editing for crop improvement is the identification of epialleles that are linked to phenotypic variation (Fig. 1). Much like the identification of genetic variation for crop improvement, looking to naturally occurring epigenomic variation provides an endless source of epialleles (Fig. 3). Thus, I am interested in unlocking the epigenome for crop improvement through the identification of epialleles that contribute to morphological variation within wild populations.

popGen.landscape.png

Figure 3. Discovery of epialleles under selection using population genetics. (A) Identification of polymorphic methylated cytosines and epialleles within a population. (B) Epiallele frequency spectrum provides information on demographic changes and natural selection. (C) Tajima's D – a comparison of the average number of pairwise differences with the number of segregating sites can distinguish between epialleles evolving neutrally and on evolving under a non-random process (i.e., selective sweep) relative to a genetic alleles.

References

  1. Huxley J (1942) Evolution: The Modern Synthesis. MIT Press, Cambridge, MA.

  2. Adli M (2018) The CRISPR tool kit for genome editing and beyond. Nature Communications 9:1911.

  3. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161. 

  4. Reinders J, Wulff BB, Mirouze M, Marí-Ordóñez A, Dapp M, Rozhon W, Bucher E, Theiler G, Paszkowski J (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes & Development 23:939–950.

  5. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5:e1000530.

  6. Ong-Abdullah M, Ordway JM, Jiang N, Ooi SE, Kok SY, Sarpan N, Azimi N, Hashim AT, Ishak Z, Rosli SK, Malike FA, Bakar NA, Marjuni M, Abdullah N, Yaakub Z, Amiruddin MD, Nookiah R, Singh R, Low ET, Chan KL, Azizi N, Smith SW, Bacher B, Budiman MA, Van Brunt A, Wischmeyer C, Beil M, Hogan M, Lakey N, Lim CC, Arulandoo X, Wong CK, Choo CN, Wong WC, Kwan YY, Alwee SS, Sambanthamurthi R, Martienssen RA (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525:533–537.

  7. Bewick AJ, Ji L, Niederhuth CE, Willing E-M, Hofmeister BT, Shi X, Wang L, Lu Z, Rohr NA, Hartwig B, Kiefer C, Deal RB, Schmutz J, Grimwood J, Stroud H, Jacobsen SE, Schneeberger K, Zhang X, Schmitz RJ (2016) On the origin and evolutionary consequences of gene body DNA methylation. Proceedings of the National Academy of Sciences USA 113:9111–9116.

  8. Niederhuth CE, Bewick AJ, Ji L, Alabady M, Kim KD, Page JT, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA, Egesi C, Schmutz J, Grimwood J, Jackson SA, Springer NM, Schmitz RJ (2016) Widespread natural variation of DNA methylation within angiosperms. Genome Biology 17:194.

  9. Bewick AJ, Niederhuth CE, Ji L, Rohr NA, Griffin PT, Leebens-Mack J, Schmitz RJ (2017) The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. Genome Biology 18:65.

  10. Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ (2017) Evolution of DNA methylation across insects. Molecular Biology and Evolution 34:654–665.

  11. Bewick AJ, Hofmeister BT, Powers R, Mondo SJ, Grigoriev IV, James TY, Stajich JE, Schmitz RJ (2018) Diversity of cytosine methylation across the fungal tree of life. Nature Ecology and Evolution (out to review).

  12. Springer NM, Schmitz RJ (2017) Exploiting induced and natural epigenetic variation for crop improvement. Nature Reviews Genetics 18:563–575.

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