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Verhoeven, K.

Publications and source records attributed to Verhoeven, K..

8 recordsLinked to original sources

Additive effects of environmental and demographic variation shape the repeatability of evolution across replicated experiments

The repeatability of evolution is fundamentally important for understanding the origin and diversification of life as well as for developing evolutionary forecasting tools. Repeatability is limited by stochasticity, here defined as changes that are independent of genotypic fitness effects. Over short timescales, the two main sources of stochasticity of evolutionary change are environmental stochasticity and demographic (life-history) stochasticity. Quantifying the relative importance of these two sources of stochasticity in driving fitness outcomes is crucially important for predicting evolutionary responses. To gain insights in the effects of stochasticity, five institutes replicated an evolutionary experiment exposing Caenorhabditis elegans to novel rearing conditions. Replication across the institutes led to variation in selective environments, e.g. through divergent microbiomes among institutes. Replication within institutes was done across demographic treatments that influence the potential for population-size dependent fluctuations in allele frequencies (drift) and genetic hitchhiking (draft). We found high among-institute variation in fitness outcomes, which was partially explained by variation in microbiota. Whereas lab-specific effects explained most of the variance in mean fitness, the repeatability of fitness outcomes depended more on demographic heterogeneity. Specifically, population bottlenecks resulted in high among-replicate variation in fitness. When combined, environmental and demographic stochasticity additively reduced repeatability, underlining their additive importance in developing evolutionary forecasting tools. These results further highlight the importance of statistically integrating heterogeneity in experimental evolution to identify factors constraining outcome repeatability and study replicability.

evolutionary biology↗

DNA methylation responses to stress across different plant species

O_LIChanges in environments trigger plant DNA methylation responses, potentially modulating stress responses. Studies on stress-induced DNA methylation typically focus on single species, limiting our understanding of what are general and specific responses between species. C_LIO_LIUsing reduced-representation bisulfite sequencing epiGBS, we compared DNA methylation stress-responses across seven plant species. Because methylation can be targeted at transposable elements (TEs) and because environmental plasticity may be particularly relevant in asexual species, we hypothesize that genome size and reproduction mode explain differences in methylation responses between species. C_LIO_LIWe show that enrichment of environmentally-induced methylation responses in genes and TEs is a general feature across plant species. While previous studies have emphasized methylation responses in CHH-cytosines, we observed that cytosines in all sequence contexts (CG, CHG, CHH) are equally likely to respond to stress. Larger-genome species showed a higher proportion of stress-responding cytosines, and asexual species showed more cytosines with a strong methylation response to stress than sexually responding species. C_LIO_LIOur study highlights the role of TEs in methylome plasticity and identifies causes of variation in methylome plasticity. This provides guidance to extrapolating results from models to other plant species, and may contribute to better understanding of functionality of the response. C_LI

plant biology↗

DNA methylation in clonal Duckweed lineages (Lemna minor L.) reflects current and historical environmental exposures.

While some DNA methylation variants are transgenerationally stable in plants, DNA methylation modifications that are specifically induced by environmental exposure are typically transient and subject to resetting in germ lines, limiting the potential for transgenerational epigenetics stress memory. Asexual reproduction circumvents germlines, and may be more conducive to long-term memory and inheritance of epigenetic marks. This, however, has been poorly explored. Taking advantage of the rapid clonal reproduction of the common duckweed Lemna minor, we tested the hypothesis that a long-term, transgenerational stress memory from exposure to high temperature can be detected in DNA methylation profiles. Using a reduced representation bisulfite sequencing approach (epiGBS), we show that high temperature stress induces DNA hypermethylation at many cytosines in CG and CHG contexts but not in CHH. In addition, a subset of the temperature responsive CHG cytosines, showed differential DNA methylation between in lineages exposed to 30{degrees}C and 24{degrees}C, 3-12 clonal generations after subsequent culturing in a common environment, demonstrating a memory effect of stress that persists over many clonal generations and that is reflected in DNA methylation. Structural annotation revealed that this memory effect in CHG methylation was enriched in TEs. We argue that the observed epigenetic stress memory is likely caused by stable transgenerational persistence of high temperature-induced DNA methylation variants across multiple clonal generations. To the extent that such epigenetic memory has functional consequences for gene expression and phenotypes, this result suggests potential for long-term modulation of stress responses in asexual plants and vegetatively propagated crops.

evolutionary biology↗

Combining epiGBS markers with long read transcriptome sequencing to assess differentiation associated with habitat in Reynoutria (aka Fallopia)

Despite the limitations of genetic bottlenecks, several invasive species appear to thrive in non-native ranges with extremely low levels of sequence-based genetic variation. We previously demonstrated differentiation of DNA methylation to habitat types of the highly clonal, genetically depauperate Japanese knotweeds using anonymous markers, but the functional relevance of this DNA methylation variation is unknown. Here, we sequenced the full transcriptome combined with a reduced representation bisulfite sequencing approach, epigenotyping by sequencing (epiGBS), to characterize the association among DNA methylation, functional transcripts and the diverse habitat types occupied by the invasive Reynoutria species. We identified 50,435 putative transcripts overall, of which 48,866 were annotated with the NCBI NR database. Of these 17,872 (35%) and 16,122 (32%) transcripts shared sequence identity with Arabidopsis thaliana and Beta vulgaris, respectively. We found genetic differentiation by habitat type suggesting the action of selection and a marginal pattern of differentiation of DNA methylation among habitats, which appears to be associated with sequence differences. However, we found no individual methylation loci associated with habitat, limiting our ability to make functional interpretations. Regardless of the source of variation in DNA methylation, these changes may represent an important component of the response to environmental conditions, particularly in highly clonal plants, but more fine scale genomics analysis is required to test if DNA methylation variation in this system is responsible for functional divergence.

plant biology↗

AlphaBeta: Computational inference of epimutation rates and spectra from high-throughput DNA methylation data in plants

IntroductionHeritable changes in cytosine methylation can arise stochastically in plant genomes independently of DNA sequence alterations. These so-called spontaneous epimutations appear to be a byproduct of imperfect DNA methylation maintenance during mitotic or meitotic cell divisions. Accurate estimates of the rate and spectrum of these stochastic events are necessary to be able to quantify how epimutational processes shape methylome diversity in the context of plant evolution, development and aging. MethodHere we describe AlphaBeta, a computational method for estimating epimutation rates and spectra from pedigree-based high-throughput DNA methylation data. The approach requires that the topology of the pedigree is known, which is typically the case in the experimental construction of mutation accumulation lines (MA-lines) in sexually or clonally reproducing species. However, this method also works for inferring somatic epimutation rates in long-lived perennials, such as trees, using leaf methylomes and coring data as input. In this case, we treat the tree branching structure as an intra-organismal phylogeny of somatic lineages and leverage information about the epimutational history of each branch. ResultsTo illustrate the method, we applied AlphaBeta to multi-generational data from selfing- and asexually-derived MA-lines in Arabidopsis and dandelion, as well as to intra-generational leaf methylome data of a single poplar tree. Our results show that the epimutation landscape in plants is deeply conserved across angiosperm species, and that heritable epimutations originate mainly during somatic development, rather than from DNA methylation reinforcement errors during sexual reproduction. Finally, we also provide the first evidence that DNA methylation data, in conjunction with statistical epimutation models, can be used as a molecular clock for age-dating trees. ConclusionAlphaBeta faciliates unprecedented quantitative insights into epimutational processes in a wide range of plant systems. Software implementing our method is available as a Bioconductor R package at http://bioconductor.org/packages/3.10/bioc/html/AlphaBeta.html

genomics↗

Experimental design for large scale omic studies

Molecular phenotyping has expanded from small sample sizes to larger complex studies and are now a common element in genetic studies. When large scale studies add a molecular phenotyping component, balancing omics batches for the factors of interest (e.g. treatment), regardless of the initial sample collection strategy always improves power. Where possible, confounding sources of experimental error that are not of interest (sample collection blocks and data collection plates) improves power as does planning batches for molecular phenotyping based on constraints during initial sample collection. Power for testing differences in molecular phenotypes is always higher when accounting for the entire experimental design during modeling. The inclusion of metadata that tracks sources variation is critical to our shared goals of enabling reproducible research.

genetics↗

Reduced-representation bisulfite sequencing finds novel epigenome-wide response to oil pollution in the foundation plant Spartina alterniflora

Theory predicts that environmental challenges can shape the composition of populations, which is manifest at the molecular level. Previously, we demonstrated that oil pollution affected gene expression patterns and altered genetic variation in natural populations of the foundation salt marsh grass, Spartina alterniflora. Here, we used a reduced representation bisulfite sequencing approach, epigenotyping by sequencing (epiGBS), to examine relationships among DNA sequence, DNA methylation, gene expression, and exposure to oil pollution. We documented genetic and methylation differentiation between oil-exposed and unexposed populations, suggesting that the Deepwater Horizon oil spill may have selected on genetic variation, and either selected on epigenetic variation or induced particular epigenotypes and expression patterns in exposed compared to unexposed populations. In support of the potential for differential response to the Deepwater Horizon oil spill, we demonstrate genotypic differences in response to oil under controlled conditions. Overall, these findings demonstrate genetic variation, epigenetic variation and gene expression are correlated to exposure to oil pollution, which may all contribute to the response to environmental stress.

ecology↗

Small RNAs reflect grandparental environments in apomictic dandelion

Plants can show long-term effects of environmental stresses and in some cases a stress memory has been reported to persist across generations, potentially mediated by epigenetic mechanisms. However, few documented cases exist of transgenerational effects that persist for multiple generations and it remains unclear if or how epigenetic mechanisms are involved. Here we show that the composition of small regulatory RNAs in apomictic dandelion lineages reveals a footprint of drought stress and salicylic acid treatment experienced two generations ago. Overall proportions of 21nt and 24nt RNA pools were shifted due to grandparental treatments. While individual genes did not show strong up- or downregulation of associated sRNAs, the subset of genes that showed the strongest shifts in sRNA abundance was significantly enriched for several GO terms including stress-specific functions. This indicates that a stress-induced signal was transmitted across multiple unexposed generations leading to persistent and functional changes in epigenetic gene regulation.

genetics↗