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.
Highlights
The 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
Identification and phylogeny of methyltransferases in S. senegalensis A search for sequences encoding sole Dnmts in the SoleaDB [34] resulted in 25 putative transcripts, which corresponded to six unique transcripts that were named, dnmt1, dnmt3aa, dnmt3ab, dnmt3ba, dnmt3bb.1 and dnmt3bb.2 in agreement with Ensembl nomenclature for orthologues
Amino acid sequence identities between dnmt1 and dnmt3 paralogs were in the range of 11.0–13.7%
Summary
The 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. DNA methylation is a key regulatory mechanism during embryonic development. The Dnmt enzymes are more diverse (with three genes in mammals Dnmt3a, Dnmt3b and Dnmt3L) and are responsible for de novo DNA methylation in germ cells and in preimplantation embryos [8, 11, 12]. De novo methylation is an essential mechanism of plant and animal development, during tissue differentiation when cells undergo epigenetic reprogramming to adopt a new phenotype [13, 14]. The teleost specific whole genome duplication has increased the dnmt copy number and six dnmt paralogs have been identified in Danio rerio [15,16,17]. The consequences during development of the extra gene copies of dnmt in fish remains to be established
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