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      DNA Methylation in Basal Metazoans: Insights from Ctenophores

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          Abstract

          Epigenetic modifications control gene expression without altering the primary DNA sequence. However, little is known about DNA methylation in invertebrates and its evolution. Here, we characterize two types of genomic DNA methylation in ctenophores, 5-methyl cytosine (5-mC) and the unconventional form of methylation 6-methyl adenine (6-mA). Using both bisulfite sequencing and an ELISA-based colorimetric assay, we experimentally confirmed the presence of 5-mC DNA methylation in ctenophores. In contrast to other invertebrates studied, Mnemiopsis leidyi has lower levels of genome-wide 5-mC methylation, but higher levels of 5-mC methylation in promoters when compared with gene bodies. Phylogenetic analysis showed that ctenophores have distinct forms of DNA methyltransferase 1 (DNMT1); the zf-CXXC domain type, which localized DNMT1 to CpG sites, and is a metazoan specific innovation. We also show that ctenophores encode the full repertoire of putative enzymes for 6-mA DNA methylation, and these genes are expressed in the aboral organ of Mnemiopsis. Using an ELISA-based colorimetric assay, we experimentally confirmed the presence of 6-mA methylation in the genomes of three different species of ctenophores, M. leidyi, Beroe abyssicola, and Pleurobrachia bachei. The functional role of this novel epigenomic mark is currently unknown. In summary, despite their compact genomes, there is a wide variety of epigenomic mechanisms employed by basal metazoans that provide novel insights into the evolutionary origins of biological novelties.

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          Author and article information

          Journal
          Integr Comp Biol
          Integr. Comp. Biol
          icb
          icbiol
          Integrative and Comparative Biology
          Oxford University Press
          1540-7063
          1557-7023
          December 2015
          14 July 2015
          : 55
          : 6
          : 1096-1110
          Affiliations
          *The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St Augustine, FL 32080, USA;
          Department of Neuroscience and McKnight Brain Institute, University of Florida, Gainesville, FL 32611, USA
          Author notes

          From the symposium “Origins of Neurons and Parallel Evolution of Nervous Systems: The Dawn of Neuronal Organization” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2015 at West Palm Beach, Florida.

          Article
          PMC4817592 PMC4817592 4817592 icv086
          10.1093/icb/icv086
          4817592
          26173712
          a82786ce-7fff-4413-9ddc-ac5d1d67bbe9
          © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.
          Page count
          Pages: 15
          Categories
          Origins of Neurons and Parallel Evolution of Nervous Systems: The Dawn of Neuronal Organization

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