Phylogeny, expression patterns and regulation of DNA Methyltransferases in early development of the flatfish, Solea senegalensis

Abstract

BackgroundThe identification of DNA methyltransferases (Dnmt) expression patterns during development and their regulation is important to understand the epigenetic mechanisms that modulate larval plasticity in marine fish. In this study, dnmt1 and dnmt3 paralogs were identified in the flatfish Solea senegalensis and expression patterns in early developmental stages and juveniles were determined. Additionally, the regulation of Dnmt transcription by a specific inhibitor (5-aza-2′-deoxycytidine) and temperature was evaluated.ResultsFive paralog genes of dnmt3, namely dnmt3aa, dnmt3ab, dnmt3ba, dnmt3bb.1 and dnmt3bb.2 and one gene for dnmt1 were identified. Phylogenetic analysis revealed that the dnmt gene family was highly conserved in teleosts and three fish-specific genes, dnmt3aa, dnmt3ba and dnmt3bb.2 have evolved. The spatio-temporal expression patterns of four dnmts (dnmt1, dnmt3aa, dnmt3ab and dnmt3bb.1) were different in early larval stages although all of them reduced expression with the age and were detected in neural organs and dnmt3aa appeared specific to somites. In juveniles, the four dnmt genes were expressed in brain and hematopoietic tissues such as kidney, spleen and gills. Treatment of sole embryos with 5-aza-2′-deoxycytidine down-regulated dntm1 and up-regulated dntm3aa. Moreover, in lecithotrophic larval stages, dnmt3aa and dnmt3ab were temperature sensitive and their expression was higher in larvae incubated at 16 °C relative to 20 °C.ConclusionFive dnmt3 and one dnmt1 paralog were identified in sole and their distinct developmental and tissue-specific expression patterns indicate that they may have different roles during development. The inhibitor 5-aza-2′-deoxycytidine modified the transcript abundance of dntm1 and dntm3aa in embryos, which suggests that a regulatory feedback mechanism exists for these genes. The impact of thermal regime on expression levels of dnmt3aa and dnmt3ab in lecithotrophic larval stages suggests that these paralogs might be involved in thermal programing.Electronic supplementary materialThe online version of this article (doi:10.1186/s12861-017-0154-0) contains supplementary material, which is available to authorized users.

DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus

“…This hypothesis matches the situation in D. rerio where DNMT1 is found with high abundance in the unfertilized egg (Fang et al., ). High expression levels of rivulus DNMT1 mRNA in early stages, from fertilized oocytes to epiboly, might show a maternal origin and is reminiscent of the situation in other fish species (Dasmahapatra & Khan, ; Firmino et al., ). Up‐regulation of DNMT3av2 from the otic lens formation stage till hatching is similar to other fish (Dasmahapatra & Khan, ; Fang et al., ; Firmino et al., ) where DNMT3a is implicated in lens formation (Seritrakul & Gross, ), neurogenesis (Firmino et al., ), and organogenesis (Takayama et al., ).…”

“…High expression levels of rivulus DNMT1 mRNA in early stages, from fertilized oocytes to epiboly, might show a maternal origin and is reminiscent of the situation in other fish species (Dasmahapatra & Khan, ; Firmino et al., ). Up‐regulation of DNMT3av2 from the otic lens formation stage till hatching is similar to other fish (Dasmahapatra & Khan, ; Fang et al., ; Firmino et al., ) where DNMT3a is implicated in lens formation (Seritrakul & Gross, ), neurogenesis (Firmino et al., ), and organogenesis (Takayama et al., ). Based on these results, as in zebrafish (Campos et al., ), we suggest that DNMT3a and DNMT3b play different roles, and we hypothesize that some level of erasure and repatterning of de novo CpG DNA methylation might be taking place early in embryogenesis (Figure ) with DNMT3bv1 , and later during the remethylation phase with DNMT3av2.…”

“…DNMT3bv1 and DNMT3a share, indeed, a DNA-binding domain and have a molecular size similar to what has been observed in their mammalian orthologues and cluster into the two main clades known in mammals as DNMT3a and DNMT3b (Turek-Plewa & Jagodzinski, 2005). In contrast, DNMT3bv2/3 could be related to DNMT3ba, a fish-specific DNMT3 gene lineage subclade (Campos et al, 2012;Dasmahapatra & Khan, 2015;Firmino et al, 2017;Shimoda, Yamakoshi, Miyake, & Takeda, 2005;Takayama, Shimoda, Takanaga, Hozumi, & Kikuchi, 2014) that result from fish-specific duplication. Moreover, as in zebrafish, frogs, and chickens, extensive searches against the putative dnmt3l in K. marmoratus have failed suggesting that this gene likely appear during the mammalian evolution and might be associated with the evolution of genomic imprinting (Campos et al, 2012).…”

The round goby genome provides insights into mechanisms that may facilitate biological invasions

“…DNA methylation dynamics in the germline follows distinct and non-mammalian patterns in zebrafish [147,148], mangrove fish [149], and medaka [150], and copy number variations in the de novo DNA methyltransferase DNMT3 in teleosts do not reflect teleost genome duplication events [116]. Together with distinct spatiotemporal expression patterns particularly during development [151][152][153][154], the peculiarities of the fish DNA methylation machinery clearly warrant an in-depth and species-aware exploration of the role of DNA methylation in fish.…”

Genome Survey of Chromatin-Modifying Enzymes in Threespine Stickleback: A Crucial Epigenetic Toolkit for Adaptation?

“…For instance, an increasing number of studies show an influence of epigenetic modifications in developmental plasticity of trout and salmon, which have implications for species-specific conservation through hatchery rearing programs (Le Luyer et al, 2017;Gavery et al, 2019). Despite the increasing availability of teleost genomic resources, the comparative biology of teleost epigenetic mechanisms remains limited, particularly for nonmodel species and wild populations (Metzger and Schulte, 2016;Firmino et al, 2017;Labbé et al, 2017;Best et al, 2018;Fellous et al, 2018Fellous et al, , 2019aTodd et al, 2019). Hence, our ability to assess the role of epigenetic modifications in adaptive potential and population persistence of ecologically relevant species is still in its infancy.…”