Intronic Non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees

Cingolani, Pablo; Cao, Xiaoyi; Khetani, Radhika S.; Chen, Chieh Chun; Coon, Melissa; Sammak, Alya’a; Bollig‐Fischer, Aliccia; Land, Susan; Huang, Yun; Hudson, Matthew E.; Garfinkel, Mark D.; Zhong, Sheng; Robinson, Gene E.; Ruden, Douglas M.

doi:10.1186/1471-2164-14-666

Cited by 66 publications

(108 citation statements)

References 60 publications

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“…3E). This result may limit the role of DNA methylation in regulating phenotype-associated gene expression or alternative splicing in our species, and contrasts with what has been described in the honey bee (26,(35)(36)(37)(38)(39).…”

Section: No Distinct Methylation Patterning Across the Genome Or Betweencontrasting

confidence: 52%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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Section: No Distinct Methylation Patterning Across the Genome Or Betweencontrasting

confidence: 52%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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“…Cingolani et al (2013) additionally analysed 5hmC in the bee genome for the first time and found it to be mostly located in introns (Cingolani et al, 2013). They furthermore described large differences in the amount -but not distribution -of 5mC between different subspecies of honey bees (africanised and european honey bees) (Cingolani et al, 2013). Similar differences in global methylation levels were observed between gametes and larvae compared to adults (Ikeda et al, 2011;Drewell et al, 2014) and between bee castes (Shi et al, 2011).…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 57%

“…5mC followed by either A, T or C) is also more abundant than CpG methylation in mammalian brains (Lister et al, 2013). Cingolani et al (2013) additionally analysed 5hmC in the bee genome for the first time and found it to be mostly located in introns (Cingolani et al, 2013). They furthermore described large differences in the amount -but not distribution -of 5mC between different subspecies of honey bees (africanised and european honey bees) (Cingolani et al, 2013).…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 99%

“…both Shi et al (2013) and Cingolani et al (2013) described 5mC to be enriched in introns over exons. Despite disagreement about the specific distribution of 5mC in bees it is established that gene body methylation is predominant, as it is in other invertebrates (Zemach et al, 2010;Lyko et al, 2010;Shi et al, 2013;Cingolani et al, 2013).…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 99%

“…Despite disagreement about the specific distribution of 5mC in bees it is established that gene body methylation is predominant, as it is in other invertebrates (Zemach et al, 2010;Lyko et al, 2010;Shi et al, 2013;Cingolani et al, 2013). Furthermore Cingolani et al (2013) showed that -both in their own dataset and in a re-analysis of Lyko et al (2010) using several different bioinformatic approaches -CHH methylation (i.e. 5mC followed by two bases which are either A, T or C) was about 5x as abundant as CpG methylation in bee brains.…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 99%

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DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

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Memory formation is a crucial task of the brain. It allows animals to dynamically respond to a changing environment by combining information about current and previous experiences. Thus, it promotes complex behaviours such as living in social groups and elaborate foraging tactics. The ability to form memories is present across the animal kingdom in a variety of forms. The honeybee -an eusocial insect -is capable of both 'simple' associative and complex rule learning. Despite decades of research into the mechanisms of memory formation, however, much remains unknown.One little-understood aspect is the regulation of molecular mechanisms during memory formation.Understanding regulation of transcription is particularly important in this context, as transcription is a requirement for any stable memory. Epigenetic mechanisms regulate transcription by directly interacting with chromatin. Importantly, epigenetic mechanisms are conserved across species as distinct as humans and honeybees. This thesis aims to investigate one particular epigenetic mechanism -DNA methylation -and its role in honey bee memory formation by using behavioural, physiological and molecular assays.First, I studied the role of DNA methyltransferases (Dnmts), which catalyse DNA methylation, after olfactory reward learning. Bees were trained to associate an odour with a sugar reward. Dnmts were then blocked after conditioning using a pharmacological inhibitor. 24 hours later, bees were tested for memory retention and generalisation. Dnmt inhibition increased the generalisation to an odour that was not present during the training, thus impairing stimulus-specific memory. This effect was learning-dependent, as bees' response to odours or sugar water alone did not change after treatment. Furthermore, this effect was robust against alterations in the training paradigm, but the directionality depended on the number of training trials. Next, I used Ca2+ -imaging of the bees' primary olfactory centre (i.e. antennal lobe, AL) to investigate whether Dnmts affect changes in AL processing established during memory formation. The AL is involved in odour discrimination and olfactory learning; both processes are also crucial for stimulus-specific memory formation. If Dnmts were inhibited after olfactory reward learning, the AL response to a new odour changed 48 hours later. This effect potentially serves as a functional explanation for the behavioural phenotype observed after Dnmt inhibition. Furthermore, this study provides the first in vivo evidence for Dnmt-mediated regulation of neuronal networks during memory formation.As DNA methylation regulates transcription, I next investigated the effect of Dnmt inhibition on gene expression. Using qPCR I studied 30 memory-associated genes. In response to Dnmt inhibition, 9 genes were upregulated after conditioning. For some of these genes I then investigated their i methylation patterns using a bisulfite conversion based Mass spectrometry approach. Memory formation changed the methylation pattern compared to both...

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Epigenetics of Aggression

Duclot

Kabbaj

2021

Current Topics in Behavioral Neurosciences

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Intronic Non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees

Cited by 66 publications

References 60 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

DNA methylation and the regulation of stimulus-specific memory formation

Epigenetics of Aggression

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