Ecological divergence of wild strawberry DNA methylation patterns at distinct spatial scales

Kort, Hanne De; Panis, Bart; Deforce, Dieter; Nieuwerburgh, Filip Van; Honnay, Olivier

doi:10.1111/mec.15689

Cited by 30 publications

(46 citation statements)

References 63 publications

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“…Library preparation, bisulfite conversion and whole-genome sequencing occurred following De Kort et al 2020 6 . Briefly, paired-end sequencing was performed on 30 whole genome DNA fragment libraries obtained after DNA extraction and sonication, rendering 76 417 704 ± 13 837 490 high quality reads (mean ± standard deviation) per sample of 75 bp.…”

Section: Whole-genome Bisulfite Sequencing and Methylation Profilingmentioning

confidence: 99%

“…Methylkit v1.10.0 42 was used to call significant differentially methylated cytosines (DMCs), which were deemed significant where (i) at least 3 samples per population had a minimum cytosine coverage of 5x, (ii) at least a 25% difference in methylation between populations was observed, and (iii) q-values <0.01. DMCs were called (see De Kort et al 2020 6 to demonstrate that alternative DMC calling parameters do not considerably affect methylation patterns). We adopted a missing data threshold of 6.9% (max.…”

Section: Whole-genome Bisulfite Sequencing and Methylation Profilingmentioning

confidence: 99%

“…Quantitative genetics theory predicts that the probability of populations to keep pace with environmental change increases with molecular variation underlying phenotypic traits affecting fitness [1][2][3] . While heritable genetic variation is thought to be the dominant driver of trait evolution, a rising number of studies suggests an important role for epigenetic variation and nongenetic inheritance in governing adaptive trait-environment covariation [4][5][6] . It remains elusive, however, to what extent genetic variation dictates epigenetic responses to environmental changes 7 .…”

Section: Introductionmentioning

confidence: 99%

“…Epigenetic variation may contribute disproportionally to adaptive evolution where the amount of standing genetic diversity is low, for example in clonal species, following demographic bottlenecks, and/or where selection pressures are variable or extremely high [31][32][33][34][35][36][37] . A recent study comparing population epigenomic signatures between a steep altitudinal gradient and a much wider continental gradient in the clonal species Fragaria vesca (woodland strawberry), demonstrated that genomic islands of epigenetic divergence readily arise even at fine spatial scale (<2km), and persist through the next generation 6 . How these epigenetic patterns behave relative to genetic variation nevertheless remains an open question that is key to understanding the molecular basis of adaptive evolution.…”

Section: Introductionmentioning

confidence: 99%

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Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Toivainen

Nieuwerburgh

et al. 2021

Preprint

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Adaptive evolution is generally thought to be the result of natural selection predominantly acting upon pre-existing DNA sequence polymorphisms through gene-environment interactions. Epigenetic inheritance is, however, recently considered an additional molecular force driving adaptive evolution independent of DNA sequence variation. Through comparative analyses of genome-wide genetic (SNPs) and epigenetic (DMCs) variation of wild strawberry plants raised under distinct drought settings, we demonstrate intermediate levels of genome-wide covariation between SNPs and DMCs. Cases of high SNP-DMC covariation were significantly associated with (i) applied stress, (ii) non-adaptive SNPs, and (iii) solitary DMCs (as opposed to DMC islands). We also found that DMCs, drought-responsive DMCs in particular, typically co-vary with hundreds of SNPs, indicating high genomic redundancy as a basis for polygenic adaptation. Our findings suggest that stress-responsive DMCs initially co-vary with many associated SNPs under increased environmental stress (cfr. co-gradient plasticity), and that natural selection acting upon these SNPs subsequently reduce standing covariation with stress-responsive DMCs. In addition, the degree of covariation between SNPs and DMCs appears independent of their respective genomic distance, indicating that trans-acting associations between SNPs and DMCs are as likely as cis-acting associations. Our study is in favor of DNA methylation profiles representing complex quantitative traits rather than independent evolutionary forces, but further research is required to fully rule out SNP-independence of genome-wide DMCs. We provide a conceptual framework for polygenic regulation and adaptation shaping genome-wide methylation patterns.

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Section: Whole-genome Bisulfite Sequencing and Methylation Profilingmentioning

confidence: 99%

Section: Whole-genome Bisulfite Sequencing and Methylation Profilingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Toivainen

Nieuwerburgh

et al. 2021

Preprint

Self Cite

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“…Additionally, inheritance of epigenetic variation has been observed in A. thaliana (Lang-Mladek et al, 2010; Blevins et al, 2014) as well as in several crop species (e.g. DNA methylation in maize and Fragaria vesca ; Li et al, 2014; de Kort et al, 2020; and small RNAs in Brassica rapa ; Bilichak et al, 2014). Our understanding of how epigenetic variation behaves in ecological contexts is far more limited, however.…”

Section: Introductionmentioning

confidence: 99%

Inheritance of DNA methylation differences in the mangrove Rhizophora mangle

Mounger

Boquete

Schmid³

et al. 2020

Preprint

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The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and non-genetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the non-genetic contributions to variation. Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions, and is potentially threatened by climate change. Several studies have documented landscape level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of non-genetic variation. To assess one type of non-genetic variation, we examined the patterns of DNA sequence and DNA methylation in maternal plants and offspring from natural populations of R. mangle from the Gulf Coast of Florida. We used a reduced representation bisulfite sequencing approach (epi-genotyping by sequencing or epiGBS) to address the following questions: a) What are the levels of genetic and epigenetic diversity in natural populations of R. mangle? b) How are genetic and epigenetic variation structured within and among populations? c) How faithfully is epigenetic variation inherited? We found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field and that a large portion (up to ~25%) of epigenetic differences among offspring grown in common garden was explained by maternal family. Therefore, epigenetic variation could be an important source of response to challenging environments in the genetically depauperate populations of this foundation species.

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(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

Chen

et al. 2022

Ecological Applications

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Elucidating processes and mechanisms involved in rapid local adaptation to varied environments is a poorly understood but crucial component in management of invasive species. Recent studies have proposed that genetic and epigenetic variation could both contribute to ecological adaptation, yet it remains unclear on the interplay between these two components underpinning rapid adaptation in wild animal populations. To assess their respective contributions to local adaptation, we explored epigenomic and genomic responses to environmental heterogeneity in eight recently colonized ascidian (Ciona intestinalis) populations at a relatively fine geographical scale. Based on MethylRADseq data, we detected strong patterns of local environment‐driven DNA methylation divergence among populations, significant epigenetic isolation by environment (IBE), and a large number of local environment‐associated epigenetic loci. Meanwhile, multiple genetic analyses based on single nucleotide polymorphisms (SNPs) showed genomic footprints of divergent selection. In addition, for five genetically similar populations, we detected significant methylation divergence and local environment‐driven methylation patterns, indicating the strong effects of local environments on epigenetic variation. From a functional perspective, a majority of functional genes, Gene Ontology (GO) terms, and biological pathways were largely specific to one of these two types of variation, suggesting partial independence between epigenetic and genetic adaptation. The methylation quantitative trait loci (mQTL) analysis showed that the genetic variation explained only 18.67% of methylation variation, further confirming the autonomous relationship between these two types of variation. Altogether, we highlight the complementary interplay of genetic and epigenetic variation involved in local adaptation, which may jointly promote populations' rapid adaptive capacity and successful invasions in different environments. The findings here provide valuable insights into interactions between invaders and local environments to allow invasive species to rapidly spread, thus contributing to better prediction of invasion success and development of management strategies.

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Ecological divergence of wild strawberry DNA methylation patterns at distinct spatial scales

Cited by 30 publications

References 63 publications

Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Inheritance of DNA methylation differences in the mangrove Rhizophora mangle

(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

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