More Than DNA Methylation: Does Pleiotropy Drive the Complex Pattern of Evolution of Dnmt1?

Amukamara, Ashley U.; Washington, Joshua T.; Sanchez, Zachary; McKinney, Elizabeth C.; Moore, Allen J.; Schmitz, Robert J.; Moore, Patricia J.

doi:10.3389/fevo.2020.00004

Cited by 21 publications

(42 citation statements)

References 35 publications

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“…Potentially, the intragenic methylation of honey bees can be used to mold chromosome structure in order to play roles in basal processes necessary for cell viability, for example, cell division, genome integrity, and/or cell cycle progression (Amukamara et al, 2020 Transcript levels of the four differentially methylated genes quantified by quantitative PCR in the brain and ovary of young honey bee workers. Note that GB55278 was also found to be differentially methylated between the ovaries of QR and QL workers (Figure 2 and Table S4).…”

Section: Discussionmentioning

confidence: 99%

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

et al. 2021

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The presence of DNA methylation marks within genic intervals, also called gene body methylation, is an evolutionarily-conserved epigenetic hallmark of animal and plant methylomes. In social insects, gene body methylation is thought to contribute to behavioural plasticity, for example between foragers and nurse workers, by modulating gene expression. However, recent studies have suggested that the majority of DNA methylation is sequence-specific, and therefore cannot act as a flexible mediator between environmental cues and gene expression. To address this paradox, we examined whole-genome methylation patterns in the brains and ovaries of young honey bee workers that had been subjected to divergent social contexts: the presence or absence of the queen. Although these social contexts are known to bring about extreme changes in behavioral and reproductive traits through differential gene expression, we found no significant differences between the methylomes of workers from queenright and queenless colonies. In contrast, thousands of regions were differentially methylated between colonies, and these differences were not associated with differential gene expression in the subset of genes examined. Methylation patterns were highly similar between brain and ovary tissues and only differed in nine regions.These results strongly indicate that DNA methylation is not a driver of differential gene expression between tissues or behavioral morphs. Finally, despite the lack of difference in methylation patterns, queen presence affected the expression of all four DNA methyltransferase genes, suggesting that these enzymes have roles beyond DNA methylation. Therefore, the functional role of DNA methylation in social insect genomes remains an open question.

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Section: Discussionmentioning

confidence: 99%

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

et al. 2021

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“…Our previous work on O. fasciatus shows that the machinery for cytosine methylation is needed for successful gamete production (Bewick et al 2019; Amukamara et al 2020; Washington et al 2021). However, the genetic underpinnings of this effect remain poorly explained.…”

Section: Discussionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted February 10, 2023. ; https://doi.org/10.1101/2023.02.09.527865 doi: bioRxiv preprint formation of primary oocytes in the developing ovary, knockdown of Dnmt1 completely ablates gamete formation despite somatic ovaries developing through a normal trajectory (Amukamara et al 2020). When Dnmt1 is knocked down during a pre-meiosis stage of juvenile testis development, males emerge as adults with significantly smaller testes that have fewer developing sperm (Washington et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Cytosine methylation itself and its machinery are variably conserved across most insect lineages (Bewick et al 2017; Provataris et al 2018; Duncan et al 2022) indicating that it has functional roles for insects. One consistent function of cytosine methylation machinery of insects is a role during gamete and embryo formation (Zwier et al 2012; Schulz et al 2018, Bewick et al 2019; Amukamara et al 2020; Gegner et al 2020; Washington et al 2021; Arsala et al 2022). This role has been demonstrated through both pharmacological and genetic manipulations.…”

Section: Introductionmentioning

confidence: 99%

“…This role has been demonstrated through both pharmacological and genetic manipulations. For some species this role has been identified to be critical during meiosis specifically ( Oncopeltus fasciatus; Amukamara et al 2020, Washington et al 2021). A mechanistic understanding of cytosine methylation and its machinery’s role is needed to address why it is critical during gamete formation (Bewick et al 2019; Washington et al 2021), despite not acting as a direct mechanism of gene regulation.…”

Section: Introductionmentioning

confidence: 99%

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The critical role ofDmnt1during spermatogenesis is not predictable, but knockdown does cause pervasive differential transcription

Cunningham¹,

Shelby²,

McKinney³

et al. 2023

Preprint

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Cytosine methylation and its machinery influence the gene expression of many eukaryotes; however, insects are an exception to this general tenet despite many lineages retaining methyltransferases and methylated genomes. Here, we tested the a priori hypothesis that perturbed genetic pathways will be associated with meiosis using transcriptomics because previous our work using Oncopeltus fasciatus shows that gametogenesis is interrupted at meiosis following knockdown of DNA methyltransferase 1 (Dnmt1). Testes, which are almost exclusively contain gametes at varying stages of development, were sampled at 7-days and 14-days following knockdown of Dmnt1 using RNAi. Using microscopy, we found actively dividing spermatocysts were reduced at both sampling points. However, we found limited support of perturbation for our predicted cell cycle and meiotic pathways and only at 14-days. We found that Gene Ontology terms had no preferential enrichment for meiosis-associated genes. Following our a priori tests, we used the full dataset to uncover further candidate pathways influenced by Dnmt1 knockdown. Very few genes were differentially expressed at 7-days, but nearly half were at 14-days. We did not find strong candidate pathways for how Dnmt1 knockdown was achieving its effect through Gene Ontology term overrepresentation analysis. Given the evidence from microscopy, we propose Dnmt1 knockdown results in condensed nuclei after mitosis-meiosis transition and then cellular arrest. This explanation posits that differential gene expression is a product of comparing healthy to arrested cells and is not a targeted response.

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A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive

et al. 2021

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There is tantalizing evidence that phenotypic plasticity can buffer novel, adaptive genetic variants long enough to permit their evolutionary spread, and this process is often invoked in explanations for rapid adaptive evolution. However, the strength and generality of evidence for it is controversial. We identify a conceptual problem affecting this debate: recombination, segregation, and independent assortment are expected to quickly sever associations between genes controlling novel adaptations and genes contributing to trait plasticity that facilitates the novel adaptations by reducing their indirect fitness costs. To make clearer predictions about this role of plasticity in facilitating genetic adaptation, we describe a testable genetic mechanism that resolves the problem: genetic covariance between new adaptive variants and trait plasticity that facilitates their persistence within populations. We identify genetic architectures that might lead to such a covariance, including genetic coupling via physical linkage and pleiotropy, and illustrate the consequences for adaptation rates using numerical simulations. Such genetic covariances may also arise from the social environment, and we suggest the indirect genetic effects that result could further accentuate the process of adaptation. We call the latter mechanism of adaptation social drive, and identify methods to test it. We suggest that genetic coupling of plasticity and adaptations could promote unusually rapid ‘runaway’ evolution of novel adaptations. The resultant dynamics could facilitate evolutionary rescue, adaptive radiations, the origin of novelties, and other commonly studied processes.

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More Than DNA Methylation: Does Pleiotropy Drive the Complex Pattern of Evolution of Dnmt1?

Cited by 21 publications

References 35 publications

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

The critical role ofDmnt1during spermatogenesis is not predictable, but knockdown does cause pervasive differential transcription

A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive

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