Contribution of epigenetic variation to adaptation in Arabidopsis

Schmid, Marc W.; Heichinger, Christian; Schmid, Diana Coman; Guthörl, Daniela; Gagliardini, Valeria; Bruggmann, Rémy; Aluri, Sirisha; Aquino, Catharine; Schmid, Bernhard; Turnbull, Lindsay A.; Grossniklaus, Ueli

doi:10.1038/s41467-018-06932-5

Cited by 118 publications

(112 citation statements)

References 74 publications

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“…In this study, DNA methylation could be assessed genome-wide in a genetically uniform background. Thus, the authors were able to show that the selected epigenetic variation was independent of genetic variation (Schmid, Heichinger, et al, 2018). However, clear evidence from non-model F I G U R E 6 Genetic distance between the 701 reference sequences that were significantly (FDR < 0.05) associated with the phenotype in G. mollugo.…”

Section: Discussionmentioning

confidence: 96%

“…In this study, DNA methylation could be assessed genome‐wide in a genetically uniform background. Thus, the authors were able to show that the selected epigenetic variation was independent of genetic variation (Schmid, Heichinger, et al, ). However, clear evidence from non‐model plant species is still lacking and also the present analysis can only indirectly provide it.…”

Section: Discussionmentioning

confidence: 99%

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Evidence for rapid evolution in a grassland biodiversity experiment

et al. 2019

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In long‐term grassland experiments, positive biodiversity effects on plant productivity commonly increase with time. Subsequent glasshouse experiments showed that these strengthened positive biodiversity effects persist not only in the local environment but also when plants are transferred into a common environment. Thus, we hypothesized that community diversity had acted as a selective agent, resulting in the emergence of plant monoculture and mixture types with differing genetic composition. To test our hypothesis, we grew offspring from plants that were grown for eleven years in monoculture or mixture environments in a biodiversity experiment (Jena Experiment) under controlled glasshouse conditions in monocultures or two‐species mixtures. We used epiGBS, a genotyping‐by‐sequencing approach combined with bisulphite conversion, to provide integrative genetic and epigenetic (i.e., DNA methylation) data. We observed significant divergence in genetic and DNA methylation data according to selection history in three out of five perennial grassland species, namely Galium mollugo, Prunella vulgaris and Veronica chamaedrys, with DNA methylation differences mostly reflecting the genetic differences. In addition, current diversity levels in the glasshouse had weak effects on epigenetic variation. However, given the limited genome coverage of the reference‐free bisulphite method epiGBS, it remains unclear how much of the differences in DNA methylation was independent of underlying genetic differences. Our results thus suggest that selection of genetic variants, and possibly epigenetic variants, caused the rapid emergence of monoculture and mixture types within plant species in the Jena Experiment.

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Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

Evidence for rapid evolution in a grassland biodiversity experiment

et al. 2019

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“…Thus, we propose that memorized methylation changes, particularly changes in CG methylation that had been most prominent in gene bodies (Fig. 7), are most likely to contribute to transgenerational plasticity across mitotically grown seagrass generations, and to offer an accelerated pathway for evolutionary change (Bräutigam et al, 2013;Zhang et al, 2013;van der Graaf et al, 2015;Platt et al, 2015;Gugger et al, 2016;Schmid et al, 2018). Memory stability across asexual generations can only be addressed by tracking stress-induced methylation changes in new vegetatively grown shoots not experiencing the stress.…”

Section: Evolutionary Potential Of the Epigenetic Heat Stress Responsementioning

confidence: 93%

“…That DNA methylation memories can mediate such adaptive transgenerational plasticity was shown in the plant Polygonium persicaria, in which offspring demethylation with zebularine removed the adaptive effect of parental drought in form of longer root systems and greater biomass (Herman and Sultan, 2016). Transgenerational methylation memories were further correlated with increased salt tolerance in F1 progeny of salt-stressed Arabidopis parents (Boyko et al, 2010), a shift in flowering time in F2 and F3 progeny of Arabidopsis subjected to disturbance (Schmid et al, 2018), and with N-deficiency tolerance in F3 progeny of N-depleted rice (Oryza sativa) (Kou et al, 2011). Whether the stress-responsive methylation patterns in Z. marina are involved in the inheritance of acquired adaptive traits requires further experiments involving at least F1 progeny.…”

Section: Evolutionary Potential Of the Epigenetic Heat Stress Responsementioning

confidence: 95%

The seagrass methylome memorizes heat stress and is associated with variation in stress performance among clonal shoots

Jueterbock

Boström

Coyer

et al. 2019

Preprint

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 Evolutionary theory predicts that clonal organisms are more susceptible to extinction than sexually reproducing organisms, due to low genetic variation and slow rates of genetic evolution. However, plants that reproduce clonally are among the oldest living organisms on our planet. Here, we test the hypothesis that clonal seagrass meadows display epigenetic diversity that compensates for the lack of genetic diversity. In a clonal meadow of the seagrass Zostera marina we characterized DNA methylation among 42 shoots. We correlated methylation patterns with photosynthetic performance under exposure to, and recovery from 27°C. Here we show for the first time that methylation variation in clonal seagrass promotes variation in fitness-related traits of ecological relevance: photosynthetic performance and heat stress resilience. The recovered shoots memorized heat responsive methylation changes for >five weeks. While genotypic diversity has been shown to enhance stress resilience and invertebrate diversity in seagrass meadows composed of several genotypes, we suggest that epigenetic variation plays a similar role in clonal meadows with the potential to secure function and resilience not only of Z. marina plants, but of the entire associated ecosystem.Consequently, conservation management of clonal plants must include epigenetic variation as indicator of resilience and stability. Chefaoui RM, Duarte CM, Serrão EA. 2018. Dramatic loss of seagrass habitat under projected climate change in the Mediterranean Sea. Global Change Biology. Costanza R, Arge R, Groot R De, Farberk S, Grasso M, Hannon B, Limburg K, Naeem S, O'Neill R V, Paruelo J, et al. 1997. The value of the world ' s ecosystem services and natural capital. Nature 387: 253-260. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. 2016. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Science Advances 2: e1501340-e1501340. Dodd RS, Douhovnikoff V. 2016. Adjusting to Global Change through Clonal Growth and Epigenetic Variation. Frontiers in Ecology and Evolution 4: 1-6. Douhovnikoff V, Dodd RS. 2014. Epigenetics: a potential mechanism for clonal plant success. Plant Ecology 216: 227-233. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR. 2012. Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences of the United States of America 109: E2183-91. Duarte CM, Kennedy H, Marbà N, Hendriks I. 2013. Assessing the capacity of seagrass meadows for carbon burial: Current limitations and future strategies. Ocean and Coastal Management 83: 32-38. Duarte B, Martins I, Rosa R, Matos AR, Roleda MY, Reusch TBH, Engelen AH, Serrao EA, Pearson GA, Marques JCJ, et al. 2018. Climate change impacts on seagrass meadows and macroalgal forests: an integrative perspective on acclimation and adaptation potential. Frontiers in Marine Science 5: 190. Dubin MJ, Zhang P, Meng D, Remigereau MS, Osborne EJ, Casale FP, Drewe P, Kahles A, Jean G, Vilhjá...

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“…For evolutionary studies, Arabidopsis thaliana is an excellent model for organisms with a full-featured methylation machinery. It has a small genome, a short life cycle, and large populations that harbor methylation polymorphisms of natural [14,15,16,17] as well as artificial origin [18,19] are available.…”

Section: Introductionmentioning

confidence: 99%

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Kartal

Schmid

Grossniklaus

2019

Preprint

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The epigenome modulates the activity of genes and supports the stability of the genome. The epigenome can also contain phenotypically relevant, heritable marks that may vary at the organismic and population level. Such non-genetic standing variation may be relevant to ecological and evolutionary processes. To identify loci susceptible to selection, it is common to profile large populations at the genome scale, yet methods to perform such scans for epigenetic diversity are barely tapped. Here, we develop a scalable, information-theoretic approach to assess epigenome diversity based on Jensen-Shannon divergence (JSD) and demonstrate its practicality by measuring cell type-specific methylation diversity in the model plant Arabidopsis thaliana. DNA methylation diversity tends to be increased in the CG as compared to the non-CG (CHG and CHH) sequence context but the tissue or cell type has an impact on diversity at non-CG sites. Less accessible, more heterochromatic states of chromatin exhibit increased diversity. Genes tend to carry more single-methylation polymorphisms when they harbor gene body-like chromatin signatures and flank transposable elements (TEs). In conclusion, the analysis of DNA methylation with JSD in Arabidopsis demonstrates that the genomic location of a gene dominates its methylation diversity, in particular the proximity to TEs which are increasingly viewed as drivers of evolution. Importantly, the JSD-based approach we implemented here is applicable to any population-level epigenomic data set to analyze variation in epigenetic marks among individuals, tissues, or cells of any organism, including the epigenetic heterogeneity of cells in healthy or diseased organs such as tumors.

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Contribution of epigenetic variation to adaptation in Arabidopsis

Cited by 118 publications

References 74 publications

Evidence for rapid evolution in a grassland biodiversity experiment

Evidence for rapid evolution in a grassland biodiversity experiment

The seagrass methylome memorizes heat stress and is associated with variation in stress performance among clonal shoots

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

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