LAUSR

* Correspondence: guillaume.filion@ utoronto.ca Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Scarborough, M1C1A4 ON, Canada Chromatin is traditionally studied in the fields of DNA repair and gene regulation, not immunology. Yet, chromatin protects the genome against several types of viruses [1, 2], so it is part of the immune system of eukaryotes in a strict sense. Chromatin allows the host genome to shut down the transcription of some genes, irrespective of their sequence. In fact, it is so well designed for the task of controlling foreign genes that one may wonder whether the function of chromatin in immunity was its raison d’être [3]. The appearance of eukaryotes coincided with the expansion of a class of retrotransposons known as non-LTR [4]. Those transposable elements feature an aggressive copy-paste replication cycle that involves an RNA intermediate [3]. They are nearly absent from prokaryotic genomes, while they can represent a large fraction of eukaryotic genomes. In humans, for instance, the most abundant non-LTR retrotransposon is LINE-1 (long interspersed nuclear element 1), with approximately 85,000 full-length copies summing up to ~ 20% of the genome. The fate of non-LTR retrotransposons is somehow bound with that of eukaryotes. It is thus plausible that some features of the early eukaryotic genomes conferred increased resistance to copy-paste mobile elements, protecting the organism against their harmful effects, but also creating an evolutionary niche for their sustained existence. The chromatin of eukaryotes contains a specialized subtype called heterochromatin, loosely defined as genomic regions that are compacted and rich in repeated sequences, and where transcription is restrained [5]. Is heterochromatin responsible for the tolerance of eukaryotic genomes to retrotransposons? In modern eukaryotes, the silencing functions of chromatin are carried out by three systems: the methylation of H3K9 (the lysine residue at position 9 of histone H3), the methylation of H3K27 (the lysine residue at position 27 of histone H3), and the methylation of cytosine in the genome [5]. Here, we will look in greater depth at H3K9 methylation because H3K27 methylation is mostly involved in the regulation of developmental genes (i.e., it is not part of constitutive heterochromatin) and cytosine methylation often changed function in the evolutionary history of eukaryotes. Methylation of H3K9 is widespread among eukaryotes; more importantly, it is present in plants and animals, which belong to two distant clades called Archaeplastida and Opisthokonta, with a common ancestor near the base of all eukaryotes [6]. Either