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Sequencing Study Uncovers Clues to Evolution of Methylation in Eukaryotes

By Andrea Anderson

NEW YORK (GenomeWeb News) – By comparing cytosine methylation patterns in more than a dozen plant, animal, and fungal genomes, University of California at Berkeley researchers have gained insights into the evolution of methylation in eukaryotes. The work appeared in the early, online edition of Science yesterday.

The researchers used sequencing-based approaches to assess cytosine methylation and gene expression in five plant, seven animal, and five fungal genomes. Their results suggest the common ancestor to these organisms was capable of both gene body and transposable element methylation. Since then, though, their findings indicate that some lineages have tossed out — or lost and then re-acquired — certain methylation mechanisms, such as the ability to silence transposons through methylation.

"Our best guess, based on our data and other people's data, is that the last common ancestor sort of resembled what you see in flowering plants now," senior author Daniel Zilberman, a plant and microbial biology researcher at UC Berkeley, told GenomeWeb Daily News.

Using the Illumina GAII, the team did a combination of bisulfite and RNA sequencing experiments to examine methylation patterns and their effects on expression in the genomes of 17 plant, animal, fungal, and algal species.

When they focused on five plants — rice, the early diverging land plant species Selaginella moellendorffii and Physcomitrella patens, and the green algal species Chorella sp. NC64A and Volvox carteri — they found that methylation patterns in rice were similar to those reported previously for Arabidopsis thaliana.

All of the plant species exhibited differential methylation of transposons, Zilberman explained. Both of the early emerging plant species tested lacked gene body methylation, although such methylation was present in Chorella and, to a lesser extent, the other green algae, V. carteri.

Next, the team examined seven animal species, including six invertebrates (the flour beetle, honeybee, silk moth, anemone, fruit fly, and sea squirt) and the puffer fish. Gene body methylation patterns were similar in the honeybee, silk moth, anemone, and sea squirt, resembling those found in puffer fish and plants. The researchers didn't detect methylation in adult flour beetles or fruit fly embryos.

As expected, Zilbermain said, vertebrates had elevated methylation around transcription start sites and transposons. In contrast to land plants and vertebrates, though, the invertebrate species do not appear to use methylation to curb the expression of transposable elements.

"Our data indicate that gene body methylation is basal, predating the divergence of plants and animals around 1.6 billion years ago, while the anti-transposon function probably evolved independently in the vertebrate and plant lineages," the team wrote.

Finally, the researchers examined five fungal species. Transposable element methylation was widespread in the fungi, though the researchers only found methylation at active genes in one species, Uncinocarpus reesii, which had higher levels of methylation at more highly expressed genes.

"Our data demonstrate that extant DNA methylation systems are mosaics of conserved and derived features, and indicate that gene body methylation is an ancient property of eukaryotic genomes," Zilberman and his co-authors wrote.

Based on the plant, animal, and fungal findings, the team argued that a common ancestor to all of these lineages was likely capable of both gene body and transposable element methylation but lost (and sometimes regained) these capabilities in certain lineages during evolution.

For example, land plants and vertebrates have retained more methylation in their genomes overall than other organisms — a pattern that the researchers believe may reflect the need for sexually reproducing organisms to curb the expression of potentially damaging transposable elements. In particular, while early animal lineages lost the ability to silence transposons through methylation, Zilberman explained, vertebrates have apparently been able to establish this silencing.

On the other hand, they noted, gene body methylation has been sporadically lost in fungi and some plant and animal groups. "[G]ene body methylation is likely a double-edged sword: it is mutagenic, so whatever benefits are derived by methylating exons come at a price," the researchers concluded. "Loss of this pathway would thus be more common, and in fact has occurred early in fungal evolution and later in several plant and animal lineages."

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