Beyond transcriptional silencing: Is methylcytosine a widely conserved eukaryotic DNA elimination mechanism?

Bracht, John R.

doi:10.1002/bies.201300123

Cited by 11 publications

(7 citation statements)

References 58 publications

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“…thermophila and other ciliates use DNA elimination to remove approximately one-third of the genome, when the somatic macronucleus differentiates from the germline micronucleus. Histone 3 lysine 9 trimethylation (H3K9me3) is deposited on DNA destined for this elimination (reviewed in Bracht 51 ). Interestingly, in other ciliates, DNA methylation is used for the tagging of DNA to be eliminated.…”

Section: Discussionmentioning

confidence: 99%

Universality of the DNA methylation codes in Eucaryotes

Aliaga

Bulla

Mouahid

et al. 2019

Sci Rep

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Genetics and epigenetics are tightly linked heritable information classes. Question arises if epigenetics provides just a set of environment dependent instructions, or whether it is integral part of an inheritance system. We argued that in the latter case the epigenetic code should share the universality quality of the genetic code. We focused on DNA methylation. Since availability of DNA methylation data is biased towards model organisms we developed a method that uses kernel density estimations of CpG observed/expected ratios to infer DNA methylation types in any genome. We show here that our method allows for robust prediction of mosaic and full gene body methylation with a PPV of 1 and 0.87, respectively. We used this prediction to complement experimental data, and applied hierarchical clustering to identify methylation types in ~150 eucaryotic species covering different body plans, reproduction types and living conditions. Our analysis indicates that there are only four gene body methylation types. These types do not follow phylogeny (i.e. phylogenetically distant clades can have identical methylation types) but they are consistent within clades. We conclude that the gene body DNA methylation codes have universality similar to the universality of the genetic code and should consequently be considered as part of the inheritance system.

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Section: Discussionmentioning

confidence: 99%

Universality of the DNA methylation codes in Eucaryotes

Aliaga

Bulla

Mouahid

et al. 2019

Sci Rep

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“…The sea lamprey may have utilized programmed DNA elimination during early embryogenesis to silence the transposable elements and maintain genome stability (Smith et al 2012;Haeusser and Margolin 2012). Interestingly, programmed genome change through DNA elimination is also present in some other vertebrates, such as spotted ratfish, bandicoot and zebra finch, and DNA methylation may play an important role in this process (Bracht et al 2012;Bracht 2014). Similarly, chicken genome also exhibits relatively low genome wide DNA methylation level (Mugal et al 2015), and contains many tiny microchromosomes .…”

Section: Discussionmentioning

confidence: 99%

Genome-wide and single-base resolution DNA methylomes of the Sea Lamprey (Petromyzon marinus) Reveal Gradual Transition of the Genomic Methylation Pattern in Early Vertebrates

Zhang

Liu

Zhou

et al. 2015

Preprint

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In eukaryotes, cytosine methylation is a primary heritable epigenetic modification of the genome that regulates many cellular processes. While the whole-genome methylation pattern has been generally conserved in different eukaryotic groups, invertebrates and vertebrates exhibit two distinct patterns. Whereas almost all CpG sites are methylated in most vertebrates, with the exception of short unmethylated regions call CpG islands, the most frequent pattern in invertebrate animals is 'mosaic methylation', comprising domains of heavily methylated DNA interspersed with domains that are methylation free. The mechanism by which the genome methylation pattern transited from a mosaic to a global pattern and the role of the one or two-round whole-genome duplication in this transition remain largely elusive, partly owing to the lack of methylome data from early vertebrates. In this study, we used the whole-genome bisulfite-sequencing technology to investigate the genome-wide methylation in three tissues (heart, muscle, and sperm) from the sea lamprey, an extant Agarthan vertebrate. Analyses of methylation level and the extent of CpG dinucleotide depletion of geneencoding, intergenic and promoter regions revealed a gradual increase in the methylation level from invertebrates to vertebrates, with the sea lamprey exhibiting an intermediate position. In addition, the methylation level of the majority of CpGs was intermediate in each sea lamprey tissue, indicating a high level of heterogeneity of methylation status between individual cells. In this regard, we defined the genomic methylation pattern of sea lamprey as "global genomic DNA intermediate methylation".The methylation features in different genomic regions, such as the transcription start site (TSS) region of the gene body, exon-intron boundaries, transposons, as well as genes grouping with different expression levels, supported the gradual methylation transition hypothesis. We further discussed that the copy number difference in DNA methylation transferases and the loss of the PWWP domain and/or DNTase domain in DNMT3 sub-family enzymes may have contributed to the methylation pattern 3 transition in early vertebrates. These findings demonstrate an intermediate genomic methylation pattern between invertebrates and jawed vertebrates, providing evidence that supports the hypothesis that methylation patterns underwent a gradual transition from invertebrates (mosaic) to vertebrates (global).

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“…Similar to H3K9 methylation in Tetrahymena , cytosine methylation may lead to heterochromatin formation and induce DNA excision in stichotrichous ciliates (117). In Stylonychia, de novo cytosine methylation occurs on transposon-like elements during differentiation of the anlagen (118).…”

Section: Bodymentioning

confidence: 99%

Programmed Genome Rearrangements in the Ciliate Oxytricha

Yerlici

Landweber

2014

Microbiol Spectr

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The ciliate Oxytricha is a microbial eukaryote with two genomes, one of which experiences extensive genome remodeling during development. Each round of conjugation initiates a cascade of events that construct a transcriptionally active somatic genome from a scrambled germline genome, with considerable help from both long and small noncoding RNAs. This process of genome remodeling entails massive DNA deletion and reshuffling of remaining DNA segments to form functional genes from their interrupted and scrambled germline precursors. The use of Oxytricha as a model system provides an opportunity to study an exaggerated form of programmed genome rearrangement. Furthermore, studying the mechanisms that maintain nuclear dimorphism and mediate genome rearrangement has demonstrated a surprising plasticity and diversity of non-coding RNA pathways, with new roles that go beyond conventional gene silencing. Another aspect of ciliate genetics is their unorthodox patterns of RNA-mediated, epigenetic inheritance, that rival Mendelian inheritance. This review takes the reader through the key experiments in a model eukaryote that led to fundamental discoveries in RNA biology and pushes the biological limits of DNA processing.

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Beyond transcriptional silencing: Is methylcytosine a widely conserved eukaryotic DNA elimination mechanism?

Cited by 11 publications

References 58 publications

Universality of the DNA methylation codes in Eucaryotes

Universality of the DNA methylation codes in Eucaryotes

Genome-wide and single-base resolution DNA methylomes of the Sea Lamprey (Petromyzon marinus) Reveal Gradual Transition of the Genomic Methylation Pattern in Early Vertebrates

Programmed Genome Rearrangements in the Ciliate Oxytricha

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