Correlation between the DNA methyltransferase (Dnmt) gene family and genome-wide 5-methylcytosine (5mC) in rotifer, copepod, and fish

Kim, Bomi; Mirbahai, Leda; Mally, Angela; Chipman, J.K.; Rhee, Jae-Sung; Lee, Jae‐Seong

doi:10.1007/s13258-015-0333-y

Cited by 16 publications

(8 citation statements)

References 45 publications

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“…Phylogenetic analysis showed their divergent evolution (Dabe, Sanford, Kohn, Bobkova, & Moroz, ) indicating a role in the maintenance of DNA methylation patterns for DNMT1, and one as methyltransferases responsible for de novo establishment of DNA methylation profiles for DNMT3a/b, which might be conserved. Consistent with previous observations (Kim et al., ), our results suggest that DNMT1 is a monophyletic group with a conserved structure among metazoan (Dabe et al., ). On the other hand, rivulus DNMT3 family formed three subgroups (DNMT3bv1, DNMT3av1/v2, and DNMT3bv2/v3).…”

Section: Discussionsupporting

confidence: 93%

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

Fellous

Labed‐Veydert

Locrel

et al. 2018

Ecology and Evolution

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In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation‐associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best‐known self‐fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re‐establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten‐Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus’ peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general‐purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.

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Section: Discussionsupporting

confidence: 93%

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

Fellous

Labed‐Veydert

Locrel

et al. 2018

Ecology and Evolution

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“…The level of 5-methylcytosine in Brachionus is below reliable limits of detection by LC-MS [ 62 ], and we and others have not found DNA methyltransferases (Dnmt1, Dnmt3) in the B. manjavacas transcriptome or in other published rotifer transcriptomes or genomes [ 15 , 31 , 62 ]. However, we report here that B. manjavacas has the molecular machinery for post-translational modifications to histone tails, including histone methylation and acetylation; these modifications play an important role in regulating gene expression.…”

Section: Resultsmentioning

confidence: 94%

Genome-wide transcriptomics of aging in the rotifer Brachionus manjavacas, an emerging model system

Gribble

Welch

2017

BMC Genomics

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BackgroundUnderstanding gene expression changes over lifespan in diverse animal species will lead to insights to conserved processes in the biology of aging and allow development of interventions to improve health. Rotifers are small aquatic invertebrates that have been used in aging studies for nearly 100 years and are now re-emerging as a modern model system. To provide a baseline to evaluate genetic responses to interventions that change health throughout lifespan and a framework for new hypotheses about the molecular genetic mechanisms of aging, we examined the transcriptome of an asexual female lineage of the rotifer Brachionus manjavacas at five life stages: eggs, neonates, and early-, late-, and post-reproductive adults.ResultsThere are widespread shifts in gene expression over the lifespan of B. manjavacas; the largest change occurs between neonates and early reproductive adults and is characterized by down-regulation of developmental genes and up-regulation of genes involved in reproduction. The expression profile of post-reproductive adults was distinct from that of other life stages. While few genes were significantly differentially expressed in the late- to post-reproductive transition, gene set enrichment analysis revealed multiple down-regulated pathways in metabolism, maintenance and repair, and proteostasis, united by genes involved in mitochondrial function and oxidative phosphorylation.ConclusionsThis study provides the first examination of changes in gene expression over lifespan in rotifers. We detected differential expression of many genes with human orthologs that are absent in Drosophila and C. elegans, highlighting the potential of the rotifer model in aging studies. Our findings suggest that small but coordinated changes in expression of many genes in pathways that integrate diverse functions drive the aging process. The observation of simultaneous declines in expression of genes in multiple pathways may have consequences for health and longevity not detected by single- or multi-gene knockdown in otherwise healthy animals. Investigation of subtle but genome-wide change in these pathways during aging is an important area for future study.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3540-x) contains supplementary material, which is available to authorized users.

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“…Interestingly, DNA methylation has been proposed to serve a role in the manifestation of interval timers in other organisms (Matsuda, Numata, & Udaka, 2020). To date, there is almost no information on DNA methyltransferase rotifer genes (Dnmts) and their methylation/demethylation patterns, but Kim et al (2016) recently identified a Dnmt‐2 homologue in the genome of Brachionus koreanus . Although elucidation of these mechanisms is beyond the scope of our study, this recent finding opens the possibility of studying whether changes in the expression of Dnmt‐2 occur across generations in parallel with changes in both PSR and the expression of genes related to the induction of sexual reproduction in populations of rotifers whose habitats differ in the degree of growing‐season length environmental predictability.…”

Section: Discussionmentioning

confidence: 99%

Transgenerational effect on sexual reproduction in rotifer populations in relation to the environmental predictability of their habitats

2023

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One way to cope with predictable environmental fluctuations that affect several generations of individuals is through nongenetic transgenerational effects. Ancestors match the phenotype of their descendants to the environment the latter are expected to experience. In facultatively sexual rotifer life cycles, sex is linked to the production of diapausing eggs, which enables survival between growing seasons. In some rotifer species, sexual reproduction is inhibited several generations after diapausing eggs hatch. We hypothesised that in ponds where the growing season length is predictable, rotifer clones reproduce asexually for more generations, allowing a fuller exploitation of the growing season and maximising production of diapausing eggs at the end of the season. We tested this prediction by estimating the proportion of sexual females produced by several clones of the rotifer Brachionus plicatilis inhabiting eight ponds that vary in the predictability of the length of their growing season. Rotifer clones from more predictable ponds were unresponsive to cues that induce sexual reproduction for more generations after leaving diapause than clones from unpredictable ponds. However, clones from more unpredictable ponds did respond to these cues from early generations, probably as a way to ensure the production of diapausing eggs against the risk of an unexpectedly early end to the growing season. Significant within‐population clonal variation was observed in transgenerational responses. Our results showed that the transgenerational inhibition of sexual reproduction observed in B. plicatilis evolved in clones from habitats where the length of the growing season (i.e., the period when populations are active in the water column) is more predictable on an interannual scale. Our findings also suggest that the longer the growing season, the more prolonged the inhibition effect (i.e., it affects a greater number of asexual generations). This research shows the importance of understanding how organisms adapt to fluctuating environments through transgenerational strategies and establishes the groundwork for future studies of the regulatory mechanisms underlying the transgenerational modulation of sex in rotifers.

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Correlation between the DNA methyltransferase (Dnmt) gene family and genome-wide 5-methylcytosine (5mC) in rotifer, copepod, and fish

Cited by 16 publications

References 45 publications

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

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

Genome-wide transcriptomics of aging in the rotifer Brachionus manjavacas, an emerging model system

Transgenerational effect on sexual reproduction in rotifer populations in relation to the environmental predictability of their habitats

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