The PWWP domain and the evolution of unique DNA methylation toolkits in Hymenoptera

Kucharski, Robert; Ellis, Nancy; Jurkowski, Tomasz P.; Hurd, Paul J.; Maleszka, Ryszard

doi:10.1016/j.isci.2023.108193

Cited by 5 publications

(2 citation statements)

References 85 publications

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“…The expression of both dnmt3 paralogs maternally and in the presumptive germ cells at the same time as Ap-vasa may indicate a role for these genes in germ cell specification or maturation. Dnmt3 is a positive regulator of translation, in honeybees (Kucharski et al 2023b) and mammals (Rona et al 2016). Dnmt3 has been shown to associate with specific histone modifications through the PWWP domain (Rona et al 2016; Du et al 2015; Dhayalan et al 2010; Kucharski et al 2023b), which is also present in Ap-Dnmt3x and so it is possible that, in this context, the dnmt3 paralogs may act as regulators of germ cell specification or maintenance through transcriptional regulation.…”

Section: Discussionmentioning

confidence: 99%

“…While Ap-dnmt3a has a Cyt C5 DNA methylase domaine (Fig. S4) and is presumed to be functional as a DNA methyltransferase, Ap-dnmt3x has a PWWP motif essential for protein-protein interactions and interactions with chromatin (Kucharski et al 2023a) and a ADDz_Dnmt3 domain (Fig. S4) but this domain is lacking some of the conserved amino acid residues thought to be required for activity as a DNA methyltransferase (Walsh et al 2010).…”

Section: Discussionmentioning

confidence: 99%

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DNA methylation machinery is involved in development and reproduction in the viviparous pea aphid (Acyrthosiphon pisum)

Yoon,

Williams,

Duncan

2024

Preprint

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The pea aphid (Acyrthosiphon pisum) like the majority of extant aphids displays cyclical parthenogenesis - the ability of mothers to switch the reproductive mode of their offspring from reproducing parthenogenetically to sexually in response to environmental cues. The pea aphid genome encodes two paralogs of the de novo DNA methyltransferase gene, dnmt3a and dnmt3x. Here we show, using phylogenetic analysis, that this gene duplication event occurred at least 106 million years ago, likely after the divergence of the lineage leading to the Aphidomorpha (aphids, phylloxera and adelgids) from that leading to the scale insects (Coccoidea) and that the two paralogs are maintained in the genomes of all aphids examined. We also show that the mRNA of both dnmt3 paralogs are maternally expressed in the viviparous aphid ovary. During development both paralogs are expressed in the germ cells of embryos beginning at stage 5 and persisting throughout development. Chemical inhibition of the DNA methylation machinery leads to defects of oocytes and early stage embryos, and causes a proportion of later stage embryos to be born dead or die soon after birth. These phenotypes suggest a role for DNA methyltransferases in reproduction, consistent with that seen in other insects. Taking the vast evolutionary history of the dnmt3 paralogs, and the localization of their mRNAs in the ovary, we suggest there is a role for dnmt3a and/or dnmt3x in early development, and a role for DNA methylation machinery in the reproduction and development of the viviparous pea aphid.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

DNA methylation machinery is involved in development and reproduction in the viviparous pea aphid (Acyrthosiphon pisum)

Yoon,

Williams,

Duncan

2024

Preprint

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Inhibiting essential elements of the DNA methylation pathway negatively impacts the miRNA pathway and fitness of the whitefly Bemisia tabaci

Bidari,

Fathipour,

Riegler

et al. 2024

Pesticide Biochemistry and Physiology

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Gene body methylation evolves during the sustained loss of parental care in the burying beetle

Sarkies,

Westoby,

Kilner

et al. 2024

Nat Commun

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Epigenetic modifications, such as 5-methylcytosine (5mC), can sometimes be transmitted between generations, provoking speculation that epigenetic changes could play a role in adaptation and evolution. Here, we use experimental evolution to investigate how 5mC levels evolve in populations of biparental insect (Nicrophorus vespilloides) derived from a wild source population and maintained independently under different regimes of parental care in the lab. We show that 5mC levels in the transcribed regions of genes (gene bodies) diverge between populations that have been exposed to different levels of care for 30 generations. These changes in 5mC do not reflect changes in the levels of gene expression. However, the accumulation of 5mC within genes between populations is associated with reduced variability in gene expression within populations. Our results suggest that evolved change in 5mC could contribute to phenotypic evolution by influencing variability in gene expression in invertebrates.

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The PWWP domain and the evolution of unique DNA methylation toolkits in Hymenoptera

Cited by 5 publications

References 85 publications

DNA methylation machinery is involved in development and reproduction in the viviparous pea aphid (Acyrthosiphon pisum)

DNA methylation machinery is involved in development and reproduction in the viviparous pea aphid (Acyrthosiphon pisum)

Inhibiting essential elements of the DNA methylation pathway negatively impacts the miRNA pathway and fitness of the whitefly Bemisia tabaci

Gene body methylation evolves during the sustained loss of parental care in the burying beetle

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