Epigenetic machinery is functionally conserved in cephalopods

Macchi, Filippo; Edsinger, Eric; Sadler, Kirsten C.

doi:10.1186/s12915-022-01404-1

Cited by 11 publications

(7 citation statements)

References 117 publications

(244 reference statements)

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“…[38] Early investigators in the DNA methylation field entertained the idea that it functioned as a broad mechanism of gene silencing. This was supported by findings that methylation of regulatory elements, either when introduced by experimental manipulation [47,48] or by pathological changes, such as cancer, [49] correlated with gene silencing. This paradigm has infiltrated textbooks and prominent review articles, but there is scant evidence supporting the notion that DNA methylation plays anything but a backstage role in regulating gene expression under physiological conditions.…”

Section: Dna Methylation: Pattern and Functionmentioning

confidence: 69%

Epigenetics across the evolutionary tree: New paradigms from non‐model animals

Sadler

2022

BioEssays

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All animals have evolved solutions to manage their genomes, enabling the efficient organization of meters of DNA strands in the nucleus and allowing for nuanced regulation of gene expression while keeping transposable elements suppressed. Epigenetic modifications are central to accomplishing all these. Recent advances in sequencing technologies and the development of techniques that profile epigenetic marks and chromatin accessibility using reagents that can be used in any species has catapulted epigenomic studies in diverse animal species, shedding light on the multitude of epigenomic mechanisms utilized across the evolutionary tree. Now, comparative epigenomics is a rapidly growing field that is uncovering mechanistic aspects of epigenetic modifications and chromatin organization in non-model invertebrates, ranging from octopus to sponges. This review puts recent discoveries in the epigenetics of non-model invertebrates in historical context, and describes new insight into the patterning and functions of DNA methylation and other highly conserved epigenetic modifications.

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Section: Dna Methylation: Pattern and Functionmentioning

confidence: 69%

Epigenetics across the evolutionary tree: New paradigms from non‐model animals

Sadler

2022

BioEssays

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“…More recently, however, many studies have shifted in focus towards the potential use of methylation to determine age in wildlife. This followed the great successes in human and murine mouse models and the accumulating evidence that methylation is conserved across most vertebrate (Jarman et al ., 2015), and even invertebrate (Macchi, Edsinger & Sadler, 2022), species. Thus far, methylation clocks for age determination have been developed or tested in more than 50 species across six classes in less than 10 years, including reptiles and bird species for which other biological clocks were not suitable.…”

Section: Discussionmentioning

confidence: 99%

Biological clocks as age estimation markers in animals: a systematic review and meta‐analysis

et al. 2023

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Various biological attributes associated with individual fitness in animals change predictably over the lifespan of an organism. Therefore, the study of animal ecology and the work of conservationists frequently relies upon the ability to assign animals to functionally relevant age classes to model population fitness. Several approaches have been applied to determining individual age and, while these methods have proved useful, they are not without limitations and often lack standardisation or are only applicable to specific species. For these reasons, scientists have explored the potential use of biological clocks towards creating a universal age‐determination method. Two biological clocks, tooth layer annulation and otolith layering have found universal appeal. Both methods are highly invasive and most appropriate for post‐mortem age‐at‐death estimation. More recently, attributes of cellular ageing previously explored in humans have been adapted to studying ageing in animals for the use of less‐invasive molecular methods for determining age. Here, we review two such methods, assessment of methylation and telomere length, describing (i) what they are, (ii) how they change with age, and providing (iii) a summary and meta‐analysis of studies that have explored their utility in animal age determination. We found that both attributes have been studied across multiple vertebrate classes, however, telomere studies were used before methylation studies and telomere length has been modelled in nearly twice as many studies. Telomere length studies included in the review often related changes to stress responses and illustrated that telomere length is sensitive to environmental and social stressors and, in the absence of repair mechanisms such as telomerase or alternative lengthening modes, lacks the ability to recover. Methylation studies, however, while also detecting sensitivity to stressors and toxins, illustrated the ability to recover from such stresses after a period of accelerated ageing, likely due to constitutive expression or reactivation of repair enzymes such as DNA methyl transferases. We also found that both studied attributes have parentally heritable features, but the mode of inheritance differs among taxa and may relate to heterogamy. Our meta‐analysis included more than 40 species in common for methylation and telomere length, although both analyses included at least 60 age‐estimation models. We found that methylation outperforms telomere length in terms of predictive power evidenced from effect sizes (more than double that observed for telomeres) and smaller prediction intervals. Both methods produced age correlation models using similar sample sizes and were able to classify individuals into young, middle, or old age classes with high accuracy. Our review and meta‐analysis illustrate that both methods are well suited to studying age in animals and do not suffer significantly from variation due to differences in the lifespan of the species, genome size, karyotype, or tissue type but rather that quantitative method, patterns of inheritance, and environmental factors should be the main considerations. Thus, provided that complex factors affecting the measured trait can be accounted for, both methylation and telomere length are promising targets to develop as biomarkers for age determination in animals.

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“…However, the relationship between DNA methylation and TEs appears species-specific in most invertebrates. For instance, in molluscs, DNA methylation outside of gene bodies occurs preferentially in some young TE classes in the bivalve C. gigas , yet the TE-rich genomes of cephalopods do not show strong TE methylation [39, 41]. Likewise, among all studied annelids, the association between DNA methylation and TEs, regardless of the class, is more pronounced and perhaps unique to O. fusiformis (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Molluscs and annelids are species-rich spiralian clades with more conservatively evolving genomes [28]. In molluscs, studies of DNA methylation have primarily focused on bivalves (e.g., the oyster Crassostrea gigas) and cephalopods [36][37][38][39][40][41], revealing generally low-tomoderate methylation levels (~10% mCG). Base-resolution profiling in adult tissues with whole-genome bisulphite sequencing confirmed a mosaic 5mC landscape that concentrates in gene bodies of highly expressed genes and in young genic TEs of bivalves but not cephalopods [39,41].…”

Section: Introductionmentioning

confidence: 99%

Annelid methylomes reveal ancestral developmental and ageing-associated epigenetic erosion across Bilateria

Guynes,

Sarre,

Carrillo-Baltodano

et al. 2023

Preprint

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BackgroundDNA methylation in the form of 5-methylcytosine (5mC) is the most abundant base modification in animals. However, 5mC levels vary widely across taxa. While vertebrate genomes are hypermethylated, in most invertebrates, 5mC concentrates on constantly and highly transcribed genes (gene body methylation; GbM) and, in some species, on transposable elements (TEs), a pattern known as ‘mosaic’. Yet, the role and developmental dynamics of 5mC and how these explain interspecific differences in DNA methylation patterns remain poorly understood, especially in Spiralia, a large clade of invertebrates comprising nearly half of the animal phyla.ResultsHere, we generate base-resolution methylomes for three species with distinct genomic features and phylogenetic positions in Annelida, a major spiralian phylum. All possible 5mC patterns occur in annelids, from typical invertebrate intermediate levels in a mosaic distribution to hypermethylation and methylation loss. GbM is common to annelids with 5mC, and methylation differences across species are explained by taxon-specific transcriptional dynamics or the presence of intronic TEs. Notably, the link between GbM and transcription decays during development, and there is a gradual and global, age-dependent demethylation in adult stages. Moreover, reducing 5mC levels with cytidine analogues during early development impairs normal embryogenesis and reactivates TEs in the annelidOwenia fusiformis.ConclusionsOur study indicates that global epigenetic erosion during development and ageing is an ancestral feature of bilateral animals. However, the tight link between transcription and gene body methylation is likely important in early embryonic stages, and 5mC-mediated TE silencing probably emerged convergently across animal lineages.

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Epigenetic machinery is functionally conserved in cephalopods

Cited by 11 publications

References 117 publications

Epigenetics across the evolutionary tree: New paradigms from non‐model animals

Epigenetics across the evolutionary tree: New paradigms from non‐model animals

Biological clocks as age estimation markers in animals: a systematic review and meta‐analysis

Annelid methylomes reveal ancestral developmental and ageing-associated epigenetic erosion across Bilateria

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