Pattern of DNA Methylation in Daphnia: Evolutionary Perspective

Kvist, Jouni; Athanàsio, Camila Gonçalves; Solari, Omid Shams; Brown, James; Colbourne, John K.; Pfrender, Michael E.; Mirbahai, Leda

doi:10.1093/gbe/evy155

Cited by 51 publications

(87 citation statements)

References 80 publications

(91 reference statements)

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“…We carried out high-coverage whole-genome bisulphite sequencing (WGBS) on 14 species of arthropod and quantified the levels of DNA methylation with base-pair resolution. To examine genome-wide methylation levels we combined this data with published results from 15 additional species (Bewick et al ., 2017; Wu et al ., 2017; Kvist et al ., 2018) which were mostly sequenced at lower coverage. Estimates of genome-wide CpG methylation were then used to reconstruct ancestral methylation levels across the arthropod phylogeny.…”

Section: Resultsmentioning

confidence: 99%

“…Prior to this study, DNA methylation had been characterised across insects (Bewick et al ., 2017) but only isolated species from more basal arthropod clades had been studied (Falckenhayn et al ., 2013; Kao et al ., 2016; Kvist et al ., 2018; de Mendoza, Pflueger and Lister, 2019; Liu et al ., 2019). By examining a phylogenetically broad range of arthropod methylomes we reconstructed the trajectory of DNA methylation patterns across the phylum.…”

Section: Discussionmentioning

confidence: 99%

“…Such patterns support the proposal that gene body methylation is conserved across eukaryotes while TE methylation has been lost altogether in arthropods (Zemach et al ., 2010; Keller, Han and Yi, 2016). However some insects show considerably higher levels of genome-wide methylation (Bewick et al ., 2017), and variation in arthropod methylation levels also exists outside of insects (Kao et al ., 2016; Kvist et al ., 2018; de Mendoza, Pflueger and Lister, 2019; Liu et al ., 2019). There is also evidence of TE methylation in the desert locust Schistocerca gregaria (Lyko et al ., 2010).…”

Section: Introductionmentioning

confidence: 99%

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Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Lewis

Ross²,

Bain³

et al. 2020

Preprint

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Cytosine methylation is an ancient epigenetic modification yet its function and extent within genomes is highly variable across eukaryotes. In mammals, methylation controls transposable elements and regulates the promoters of genes. In insects, DNA methylation is generally restricted to a small subset of transcribed genes, with both intergenic regions and transposable elements (TEs) depleted of methylation. The evolutionary origin and the function of these methylation patterns are poorly understood. Here we characterise the evolution of DNA methylation across the arthropod phylum. While the common ancestor of the arthropods had low levels of TE methylation and did not methylate promoters, both of these functions have evolved independently in centipedes and mealybugs. In contrast, methylation of the exons of a subset of transcribed genes is ancestral and widely conserved across the phylum, but has been lost in specific lineages. Remarkably the same set of genes are likely to be methylated in all species that retained exon-enriched methylation. We show that these genes have characteristic patterns of expression correlating to broad transcription initiation sites and well-positioned nucleosomes, providing new insights into potential mechanisms driving methylation patterns over hundreds of millions of years.Author SummaryAnimals develop from a single cell to form a complex organism with many specialised cells. Almost all of the fantastic variety of cells must have the same sequence of DNA, and yet they have distinct identities that are preserved even when they divide. This remarkable process is achieved by turning different sets of genes on or off in different types of cell using molecular mechanisms known as “epigenetic gene regulation”.Surprisingly, though all animals need epigenetic gene regulation, there is a huge diversity in the mechanisms that they use. Characterising and explaining this diversity is crucial in understanding the functions of epigenetic pathways, many of which have key roles in human disease. We studied how one particular type of epigenetic regulation, known as DNA methylation, has evolved within arthropods. Arthropods are an extraordinarily diverse group of animals ranging from horseshoe crabs to fruit flies. We discovered that the levels of DNA methylation and where it is found within the genome changes rapidly throughout arthropod evolution. Nevertheless, there are some features of DNA methylation that seem to be the same across most arthropods-in particular we found that there is a tendency for a similar set of genes to acquire methylation of DNA in most arthropods, and that this is conserved over 350 million years. We discovered that these genes have distinct features that might explain how methylation gets targeted. Our work provides important new insights into the evolution of DNA methylation and gives some new hints to its essential functions.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Lewis

Ross²,

Bain³

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…Jones and Takai 2001). These studies have demonstrated that although there certainly are similarities between taxa in their epigenetic mechanisms and the epigenetic landscape (Law and Jacobsen 2010) there can also be substantial differences (Hunt et al 2013;Kvist et al 2018;Waters et al 2018), even within vertebrates (Jabbari et al 1997). For example, while functional DNA methylation in plants is low throughout the genome and predominantly exists in relation to transposable element (TE) activity (Hollister and Gaut 2009;Zhang 2008), most mammal DNA methylation levels are high and variation seems to be present in promoter regions of genes and TEs, directly affecting gene expression (Suzuki and Bird 2008).…”

Section: Why Study Epigenetic Effects In Birds?mentioning

confidence: 99%

Avian ecological epigenetics: pitfalls and promises

et al. 2019

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Epigenetic mechanisms can alter gene expression without a change in the nucleotide sequence and are increasingly recognized as important mechanisms that can generate phenotypic diversity. Most of our current knowledge regarding the origin and role of epigenetic variation comes from research on plants or mammals, often in controlled rearing conditions. Epigenetic research on birds in their natural habitats is still in its infancy, but is needed to answer questions regarding the origin of epigenetic marks and their role in phenotypic variation and evolution. Here we review the potential for studying epigenetic variation in natural bird systems. We aim to provide insights into (1) the origin of epigenetic variation, (2) the relationship between epigenetic variation and trait variation, and (3) the possible role of epigenetic variation in adaptation to changing environments. As there is currently little research on epigenetics in wild birds, we examine how findings on other taxa such as plants and mammals relate to birds. We also examine some of the pros and cons of the most commonly used methods to study patterns of DNA methylation in birds, and suggest some topics we believe need to be addressed to develop the field of wild avian epigenetics further. Zusammenfassung Anwendung von Epigenetik an freilebenden VögelnEpigenetische Mechanismen sind in der Lage die Aktivität eines Gens zu beeinflussen ohne die DNA-Sequenz zu veränderen und werden zunehmend als wichtige Mechanismen erkannt um phänotypische Diversität generieren zu können. Der größte Teil unseres derzeitigen Wissens über den Ursprung und die Rolle epigenetischer Variationen stammt aus der Erforschung von Pflanzen oder Säugetieren, oft unter kontrollierten Aufzuchtbedingungen. Die epigenetische Forschung an Vögeln in ihren natürlichen Lebensräumen steckt noch in den Kinderschuhen, ist jedoch erforderlich, um Fragen zur Herkunft der epigenetischen Merkmale und ihrer Rolle bei der Variation und Evolution des Phänotyps zu beantworten. Hier untersuchen wir das Potenzial zur Untersuchung der epigenetischen Variation in natürlichen Vogelsystemen. Wir möchten Einblicke geben in Communicated by M. Wink.

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“…It is also recognized that genetic, non-genetic and environmental elements interact to bring about phenotypic variation in daphnia populations (Harney et al 2017), a phenomenon that is probably applicable to all eukaryotes and that we have recently conceptualized as a systems biology view on inheritance (Cosseau et al 2016). Daphnia possess bearers of epigenetic information such as modified histones (Robichaud et al 2012), and DNA methylation (Kvist et al 2018) of the classical mosaic type (Aliaga et al 2019). Despite the the fact that the idea of a matrix was known when the term 'phenotypic plasticity' was formalised, it remains surprising that, to date, the link between Woltereck's matrix and the chromatin has not been explicitly made.…”

Section: Discussionmentioning

confidence: 99%

Chromatin structure changes inDaphniapopulations upon exposure to environmental cues – or – The discovery of Wolterecks “Matrix”

Augusto

Minoda²,

Rey

et al. 2019

Preprint

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Phenotypic plasticity is an important feature of biological systems that is likely to play a major role in the future adaptation of organisms to the ongoing global changes. It may allow an organism to produce alternative phenotypes in responses to environmental cues. Modifications in the phenotype can be reversible but are sometimes enduring and can even span over generations. The notion of phenotypic plasticity was conceptualized in the early 20 th century by Richard Woltereck. He introduced the idea that the combined relations of a phenotypic character and all environmental gradients that influence on it can be defined as "norm of reaction". Norms of reaction are specific to species and to lineages within species, and they are heritable. He postulated that reaction norms can progressively be shifted over generations depending on the environmental conditions. One of his biological models was the water-flee daphnia. Woltereck proposed that enduring phenotypic modifications and gene mutations could have similar adaptive effects, and he postulated that their molecular bases would be different. Mutations occurred in genes, while enduring modifications were based on something he called the Matrix. He suggested that this matrix (i) was associated with the chromosomes, (ii) that it was heritable, (iii) it changed during development of the organisms, and (iv) that changes of the matrix could be simple chemical substitutions of an unknown, but probably polymeric molecule. We reasoned that the chromatin has all postulated features of this matrix and revisited Woltereck's classical experiments with daphnia. We developed a robust and rapid ATAC-seq technique that allows for analyzing chromatin of individual daphnia and show here (i) that this technique can be used with minimal expertise in molecular biology, and (ii) we used it to identify open chromatin structure in daphnia exposed to different environmental cues. Our result indicates that chromatin structure changes consistently in daphnia upon this exposure confirming Woltereck's classical postulate.

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Pattern of DNA Methylation in Daphnia: Evolutionary Perspective

Cited by 51 publications

References 80 publications

Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Avian ecological epigenetics: pitfalls and promises

Chromatin structure changes inDaphniapopulations upon exposure to environmental cues – or – The discovery of Wolterecks “Matrix”

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