Metamorphosis and transition between developmental stages in European eel (Anguilla anguilla, L.) involve epigenetic changes in DNA methylation patterns

Trautner, Jochen; Reiser, Stefan; Blancke, Tina; Unger, Katrin; Wysujack, Klaus

doi:10.1016/j.cbd.2017.04.002

Cited by 8 publications

(6 citation statements)

References 67 publications

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“…On the other hand, the strong representation of developmental processes among GO terms for hypermethylated outliers supports links to metamorphic processes. Moreover, whereas our study analysed methylation in muscle tissue, a previous study of European eel using methylation‐sensitive amplified polymorphisms (MSAP) and comparing life stages found little divergence in liver tissue but larger differences in gill and brain tissues (Trautner et al, 2017). These tissue‐specific differences argue against merely age‐related effects and support methylation differences being due to specific traits and environmental conditions encountered by the life stages, for example, fresh or brackish water in yellow eels and oceanic salinities to be encountered during the spawning migration of silver eels.…”

Section: Discussionmentioning

confidence: 88%

“…The recently arrived juveniles metamorphose into so‐called glass eels, settle in freshwater and coastal marine habitats and go through an additional stage of metamorphosis until they mature as silver eels and undertake their >5000 km spawning migration back to the Sargasso Sea (Schmidt, 1923; Tesch, 2003). Previous results based on anonymous methylation markers suggest major differences between life stages (Trautner et al, 2017), but it is unknown if these differences represent functionally important methylation in relation to developmental stages or merely ageing effects (Anastasiadi & Piferrer, 2020; Horvath & Raj, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Genome‐wide methylation in the panmictic European eel (Anguilla anguilla)

et al. 2022

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The role of methylation in adaptive, developmental and speciation processes has attracted considerable interest, but interpretation of results is complicated by diffuse boundaries between genetic and non‐genetic variation. We studied whole genome genetic and methylation variation in the European eel, distributed from subarctic to subtropical environments, but with panmixia precluding genetically based local adaptation beyond single‐generation responses. Overall methylation was 70.9%, with hypomethylation predominantly found in promoters and first exons. Redundancy analyses involving juvenile glass eels showed 0.06% and 0.03% of the variance at SNPs to be explained by localities and environmental variables, respectively, with GO terms of genes associated with outliers primarily involving neural system functioning. For CpGs 2.98% and 1.36% of variance was explained by localities and environmental variables. Differentially methylated regions particularly included genes involved in developmental processes, with Hox clusters featuring prominently. Life stage (adult versus glass eels) was the most important source of inter‐individual variation in methylation, probably reflecting both ageing and developmental processes. Demethylation of transposable elements relative to pure European eel was observed in European X American eel hybrids, possibly representing postzygotic barriers in this system characterized by prolonged speciation and ongoing gene flow. Whereas the genetic data are consistent with a role of single‐generation selective responses, the methylation results underpin the importance of epigenetics in the life cycle of eels and suggest interactions between local environments, development and phenotypic variation mediated by methylation variation. Eels are remarkable by having retained eight Hox clusters, and the results suggest important roles of methylation at Hox genes for adaptive processes.

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Section: Discussionmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Genome‐wide methylation in the panmictic European eel (Anguilla anguilla)

et al. 2022

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“…In this context, previous studies have also evidenced the important effect that genome-wide DNA methylation changes have in other marine organisms with complex life-cycles involving developmental and ecological transitions. In European eel, transitions between developmental stages and new habitats (i.e., freshwater or seawater environments) were associated with different DNA methylation patterns analyzed by MSAP in gills, which is a crucial tissue for osmoregulation [ 28 ]. Similarly, smoltifying salmonids such as rainbow trout [ 25 ] and brown trout [ 24 ] showed DNA methylation-mediated epigenetic differences in branchial tissue.…”

Section: Discussionmentioning

confidence: 99%

“…This process usually implies the acquisition of new morphological, physiological and behavioral features for the adaptation to a new stage of the life cycle in a different environment [ 27 ]. In this context, global DNA methylation-mediated epigenetic changes were associated with metamorphosis and environmental transitions in European eel ( Anguilla anguilla ) [ 28 ] and lamprey ( Petromyzon marinus ) [ 29 ]. In Japanese flounder ( Paralichthys olivaceus ), the DNA methylation pattern of muscle-related genes ( smyd1a and smyd1b ) was associated to the modulation of their gene expression levels during metamorphosis [ 30 ].…”

Section: Introductionmentioning

confidence: 99%

Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement

Suárez-Bregua¹,

Rosendo²,

Comesaña³

et al. 2021

Front Zool

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Introduction Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecological transition from a pelagic to a benthonic lifestyle. Therefore, transition from a pelagic to a benthonic habitat requires multiple adaptations, however, the underlying mechanisms regulating this process still remains unclear. Epigenetic regulation and specifically DNA methylation, has been suggested to be particularly important for organisms to adapt to new environments. Seahorses (Family Syngnathidae, Genus Hippocampus) are a fascinating group of fish, distinguished by their unique anatomical features, reproductive strategy and behavior. They are unique among vertebrate species due to their “male pregnancy”, where males nourish developing embryos and larvae in a brood pouch until hatching and parturition occurs. After birth, free-swimming offspring are pelagic and subsequently they change into a demersal lifestyle. Therefore, to begin to address the question whether epigenetic processes could be involved in the transition from a planktonic to a benthonic lifestyle observed in seahorses, we studied global DNA methylation profiles in a tropical seahorse species (Hippocampus reidi) during postnatal development and settlement. Results We performed methylation-sensitive amplified polymorphism (MSAP) along with quantitative expression analysis for genes suggested to be involved in the methylation machinery at six age groups: 1, 5, 10, 20, 30 and 40 days after male’s pouch release (DAR). Results revealed that the H. reidi genome has a significantly different DNA methylation profile during postnatal development and settlement on demersal habitats. Moreover, gene expression analysis showed up- and down-regulation of specific DNA methyltransferases (DNMTs) encoding genes. Conclusion Our data show that the differences in the DNA methylation patterns seen among developmental stages and during the transition from a pelagic to a benthonic lifestyle suggest a potential for epigenetic regulation of gene expression (through DNA methylation) in this species. Therefore, epigenetic mechanisms could be necessary for seahorse settlement. Nevertheless, if these epigenetic mechanisms come from internal or if they are initiated via external environmental cues should be further investigated.

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“…This could possibly indicate a reduced preconditioning due to the lack of brackish water experience, but an almost equal part of the emigrating eels, and likely also stocked eels, (cluster 3), did not show prolonged brackish water residence. The partition of most eels into two groups of migrants might probably reflect different states of metamorphosis, as suggested in a study on DNA methylation patterns of silver eels (Trautner, Reiser, Blancke, Unger & Wysujack, 2017). Therein, silver eels from the freshwater part of River Rhine displayed two separate patterns of methylation of DNA from gills: 50% of the silver eels had "already" reached a methylation state similar to glass eels, while the other half was distinct from glass and yellow eels.…”

Section: Escapementmentioning

confidence: 91%

Behaviour, escapement and mortality of female European silver eels within a regulated lowland river draining into the Baltic Sea

Frankowski¹,

Dorow²,

Juenger

et al. 2018

Fisheries Management Eco

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Migration patterns of 146 female silver eels on their way through fresh and brackish water stretches of the Warnow River into the Baltic Sea were studied using acoustic telemetry. The majority of eels (77%) regained their expected downstream migration behaviour after a median rehabilitation time of 2 days. Positive rheotactic behaviour was observed for 23% of tagged eels after release, probably influenced by experimental procedures. The observed silver eel escapement rate was 63%. Two migratory groups were classified by significantly different migratory speed, time of residence in brackish waters and biometric silvering characteristics. Although the classification of silvering stages is based on these measures, the proportions of these stages did not reflect the observed differences in migratory behaviour. In the context of a permanent silver eel descent in the freshwater part of the Warnow River, a permanent escapement was likewise occurring into the Baltic Sea.

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Metamorphosis and transition between developmental stages in European eel (Anguilla anguilla, L.) involve epigenetic changes in DNA methylation patterns

Cited by 8 publications

References 67 publications

Genome‐wide methylation in the panmictic European eel (Anguilla anguilla)

Genome‐wide methylation in the panmictic European eel (Anguilla anguilla)

Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement

Behaviour, escapement and mortality of female European silver eels within a regulated lowland river draining into the Baltic Sea

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