Evolutionary Diversification of DNA Methyltransferases in Eukaryotic Genomes

Abstract

In eukaryotes, C5-cytosine methylation is a common mechanism associated with a variety of functions such as gene regulation or control of genomic stability. Different subfamilies of eukaryotic methyltransferases (MTases) have been identified, mainly in metazoa, plants, and fungi. In this paper, we used hidden Markov models to detect MTases in completed or almost completed eukaryotic genomes, including different species of Protozoa. A phylogenetic analysis of MTases enabled us to define six subfamilies of MTases, including two new subfamilies. The dnmt1 subfamily that includes all the known MTases with a maintenance activity seems to be absent in the Protozoa. The dnmt2 subfamily seems to be the most widespread, being present even in the nonmethylated Dictyostelium discoideum. We also found two dnmt2 members in the bacterial genus Geobacter, suggesting that horizontal transfers of MTases occurred between eukaryotes and prokaryotes. Even if the direction of transfer cannot be determined, this relationship might be useful for understanding the function of this enigmatic subfamily of MTases. Globally, our analysis reveals a great diversity of MTases in eukaryotes, suggesting the existence of different methylation systems. Our results also suggest acquisitions and losses of different MTases in every eukaryotic lineage studied and that some eukaryotes appear to be devoid of methylation.

On the origin and functions of RNA-mediated silencing: from protists to man

“…RNAi-dependent transcriptional silencing has been demonstrated to entail histone modifications, such as H3K9 methylation, in eukaryotes belonging to at least three different supergroups (Table 2). Moreover, siRNA-triggered transcriptional repression occurs in organisms that lack cytosine DNA methylation such as S. pombe and C. elegans (Grishok et al 2005;Martienssen et al 2005;Ponger and Li 2005;Robert et al 2005;Volpe et al 2002) and in organisms with very limited DNA methylation such as T. brucei and D. melanogaster (Kavi et al 2005;Pal-Bhadra et al 2004;Ponger and Li 2005;Shi et al 2004;Ullu et al 2004). In contrast, RNA-directed DNA methylation has, thus far, only been demonstrated in plants and mammals (Kawasaki and Taira 2004;Matzke and Birchler 2005;Morris et al 2004) and the role of DNA methylation in this type of gene silencing is somewhat debatable in mammals (Ting et al 2005;Weinberg et al 2006).…”

Gene silencing in microalgae: Mechanisms and biological roles

“…Introduction of a methyl group at the C5 position of cytosine is catalyzed by a large family of DNA methyltransferases, including six subfamilies characterized by catalytic domains associated with N-terminal or C-terminal extensions containing distinct motifs (Goll and Bestor, 2005;Ponger and Li, 2005;Huff and Zilberman, 2014). In land plants, DNA cytosine methylation can occur in three sequence contexts namely CG, CHG, and CHH (where H = A, T, or C) and three DNA methyltransferase subfamilies have been implicated in the establishment and/or maintenance of methylation at these sequences (Goll and Bestor, 2005;Law and Jacobsen, 2010).…”

“…Homologs of Dnmt3/DRM enzymes, which have been implicated in de novo DNA methylation (Goll and Bestor, 2005;Ponger and Li, 2005;Law and Jacobsen, 2010), were found only in the red algae Galdieria sulphuraria and Cyanidioschyzon merolae (Table 1) and with a structural organization similar to the vertebrate enzymes (data not shown), whereas chromomethylase-related methyltransferases appear to be restricted to the genus Chlorella (Table 1). Dnmt1/ MET1 homologs were identified in species of the Trebouxiophyceae (C. sorokiniana and C. variabilis) and Chlorophyceae (C. reinhardtii and V. carteri) classes (Table 1 and Fig.…”

“…Additionally, all these algal sequences contain N-terminal extensions with conserved DNMT-RFD (DNA methyltransferase replication foci domain) and BAH domains (Fig. 3), as observed in the canonical enzyme (Goll and Bestor, 2005;Ponger and Li, 2005). Figure 3.…”

Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms

“…Also, several studies have demonstrated that de novo CHH methylation could be established by the plant-specific DNA methyltransferase CMT2 in an independent RdDM pathway (Zemach et al, 2013;Stroud et al, 2014). In addition, the DNA methyltransferase-like Dnmt2, first identified from bacteria, also was detected in plants, although its function in regulating DNA methylation remained largely unknown (Hermann et al, 2003;Mund et al, 2004;Ponger and Li, 2005). According to observations of genomic DNA methylation, there is generally a substantial amount of CG methylation and a small amount of non-CG methylation, although the genomic DNA methylation level varies broadly in the plants tested (Zemach et al, 2010b).…”