Extensive DNA methylome rearrangement during early lamprey embryogenesis

Allegra Angeloni, Skye Fissette, Deniz Kaya, Jillian M. Hammond, Hasindu Gamaarachchi, Ira W. Deveson, Robert J. Klose, Weiming Li, Xiaotian Zhang and Ozren Bogdanovic ()
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Allegra Angeloni: Garvan Institute of Medical Research
Skye Fissette: Michigan State University
Deniz Kaya: University of Oxford
Jillian M. Hammond: Garvan Institute of Medical Research
Hasindu Gamaarachchi: Garvan Institute of Medical Research
Ira W. Deveson: Garvan Institute of Medical Research
Robert J. Klose: University of Oxford
Weiming Li: Michigan State University
Xiaotian Zhang: Van Andel Research Institute
Ozren Bogdanovic: Garvan Institute of Medical Research

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract DNA methylation (5mC) is a repressive gene regulatory mark widespread in vertebrate genomes, yet the developmental dynamics in which 5mC patterns are established vary across species. While mammals undergo two rounds of global 5mC erasure, teleosts, for example, exhibit localized maternal-to-paternal 5mC remodeling. Here, we studied 5mC dynamics during the embryonic development of sea lamprey, a jawless vertebrate which occupies a critical phylogenetic position as the sister group of the jawed vertebrates. We employed 5mC quantification in lamprey embryos and tissues, and discovered large-scale maternal-to-paternal epigenome remodeling that affects ~30% of the embryonic genome and is predominantly associated with partially methylated domains. We further demonstrate that sequences eliminated during programmed genome rearrangement (PGR), are hypermethylated in sperm prior to the onset of PGR. Our study thus unveils important insights into the evolutionary origins of vertebrate 5mC reprogramming, and how this process might participate in diverse developmental strategies.

Date: 2024
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DOI: 10.1038/s41467-024-46085-2

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