An epigenetic toolkit allows for diverse genome architectures in eukaryotes

Abstract

Genome architecture varies considerably among eukaryotes in terms of both size and structure (e.g. distribution of sequences within the genome, elimination of DNA during formation of somatic nuclei). The diversity in eukaryotic genome architectures and the dynamic processes that they undergo are only possible due to the well-developed nature of an epigenetic toolkit, which likely existed in the Last Eukaryotic Common Ancestor (LECA). This toolkit may have arisen as a means of navigating the genomic conflict that arose from the expansion of transposable elements within the ancestral eukaryotic genome. This toolkit has been coopted to support the dynamic nature of genomes in lineages across the eukaryotic tree of life. Here we highlight how the changes in genome architecture in diverse eukaryotes are regulated by epigenetic processes by focusing on DNA elimination, genome rearrangements, and adaptive changes to genome architecture. The ability to epigenetically modify and regulate genomes has contributed greatly to the diversity of eukaryotes observed today.

Insights into transgenerational epigenetics from studies of ciliates

“…Though the molecular mechanisms underlying epigenetic processes vary, RNA-mediated processes are emerging as a common theme across eukaryotic lineages, including ciliate lineages (Fedoroff, 2012; Maurer-Alcala and Katz, 2015; Yao et al, 2002). RNA-mediated processes (referred to here as genome scanning) involve epigenetic changes to genomes regulated by single-stranded RNAs that silence transposable elements (Chalker et al, 2013; Coyne et al, 2012; Fedoroff, 2012), generate heterochromatin (Chalker and Yao, 2011), and eliminate DNA (Fang et al, 2012; Maurer-Alcala and Katz, 2015; Swart et al, 2014).…”

“…RNA-mediated processes (referred to here as genome scanning) involve epigenetic changes to genomes regulated by single-stranded RNAs that silence transposable elements (Chalker et al, 2013; Coyne et al, 2012; Fedoroff, 2012), generate heterochromatin (Chalker and Yao, 2011), and eliminate DNA (Fang et al, 2012; Maurer-Alcala and Katz, 2015; Swart et al, 2014). …”

“…The mechanisms underlying genome scanning in ciliates and epigenetic processes in other eukaryotic lineages share similarities with transposon excision machinery (Arnaiz et al, 2012; Chalker et al, 2013; Coyne et al, 2012; Maurer-Alcala and Katz, 2015; Schoeberl and Mochizuki, 2011; Singh et al, 2014; Swart et al, 2014). For instance, in Euplotes and Paramecium species, the TA dinucleotides flanking IESs bear resemblance to the termini of Tc1/mariner transposons (Arnaiz et al, 2012; Chalker et al, 2013; Coyne et al, 2012).…”

Evolutionary origins and impacts of genome architecture in ciliates

“…Here, we describe how the atypical genome architectures in ciliates, coupled with a predominantly asexual life cycle punctuated by rare sexual events (similar to yeasts and other protists), provide them with an immense evolutionary potential and the means for rapid adaptation. This is largely due to the evolutionary impacts of ancient genome conflict with TEs, which are well known to provide the basis for evolutionary innovation in other eukaryotes . The general exploration of the interrelations between ciliate genome architecture, programmed genome rearrangements, and their life history (i.e., asexual growth with infrequent sexual events) will draw more attention to the role of genome architecture in evolution.…”

“…[1][2][3][4][5][6] While TEs are often described as parasitic or selfish DNA that are assumed to proliferate at the expense of the host genome's fitness (i.e., by increasing genome instability), 7,8 they remain essential and well-regulated genomic components, for example, possessing roles as centromeres and/or telomeres in Dictyostelium discoideum and Drosophila melanogaster, respectively. 9,10 Maintaining some control over genome instability provides massive fitness benefits to the host genome/organism, and is linked to genome dynamism, [11][12][13][14][15][16][17] which is exaggerated and well studied in pathogenic lineages (Phytophthora infestans and Entamoeba histolytica). [11][12][13] A dramatic example is the separation of germ-line and somatic genomes, which provides the means to protect the heritable genome while reaping the benefits of a highly dynamic and responsive soma.…”