Patterns of Repeat-Induced Point Mutation in Transposable Elements of Basidiomycete Fungi

Abstract

Transposable elements (TEs) are ubiquitous genomic parasites that have prompted the evolution of genome defense systems that restrict their activity. Repeat-induced point mutation (RIP) is a homology-dependent genome defense that introduces C-to-T transition mutations in duplicated DNA sequences and is thought to control the proliferation of selfish repetitive DNA. Here, we determine the taxonomic distribution of hypermutation patterns indicative of RIP among basidiomycetes. We quantify C-to-T transition mutations in particular di- and trinucleotide target sites for TE-like sequences from nine fungal genomes. We find evidence of RIP-like patterns of hypermutation at TpCpG trinucleotide sites in repetitive sequences from all species of the Pucciniomycotina subphylum of the Basidiomycota, Microbotryum lychnidis-dioicae, Puccinia graminis, Melampsora laricis-populina, and Rhodotorula graminis. In contrast, we do not find evidence for RIP-like hypermutation in four species of the Agaricomycotina and Ustilaginomycotina subphyla of the Basidiomycota. Our results suggest that a RIP-like process and the specific nucleotide context for mutations are conserved within the Pucciniomycotina subphylum. These findings imply that coevolutionary interactions between TEs and a hypermutating genome defense are stable over long evolutionary timescales.

Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus

“…Mated cells of M. lychnidis-dioicae respond to corn oil, in addition to the other lipids previously reported [45]. This supports the hypothesis that lipid response may be important for the development of this species.…”

Genome Comparison of Barley and Maize Smut Fungi Reveals Targeted Loss of RNA Silencing Components and Species-Specific Presence of Transposable Elements

“…However, this was not easily corroborated when analyzing a potential genome-wide reduction in CpG dinucleotides (see Supplemental Figure 7 online). The low abundance of repeats could compromise a proper analysis in this fungus; it was concluded previously that S. reilianum and U. maydis likely do not possess a RIP mechanism (Horns et al, 2012). In contrast with U. hordei, U. maydis lacks RNAi, HP1-like, and putative DNA methyltransferase genes, and no RIP mutation mechanism has been identified thus far.…”

Genomic and transcriptomic analyses of Microbotryum lychnidis-dioicae provide insights into the biology of a fascinating fungal phytopathogen.

“…2-8). Eighty per cent of TE copies with high frequencies of cytosine mutation showed a bias toward CpG dinucleotides, consistent with the "CpG effects" (Walser & Furano, 2010) of maintenance methylation known in eukaryotes (Fryxell & Moon, 2005;Jiang & Zhao, 2006;Morton et al, 2006), including fungi Horns et al, 2012) where CpG methylation of TEs have been shown in ascomycete and basidiomycete fungi (Zemach et al, 2010). Notably, the rate of CpG mutations varied according to TE order and superfamily examined: TE copies exhibiting a pattern of frequent transition at CpG sites appeared lower for class II DNA transposons (Helitron-type and TIR elements) than that of class I Retrotransposons (21% and 58% respectively) ( Fig.…”

“…SSPs were indeed located nearer to TEs than the set of all other non-SSP genes (Chi-squared p-value < 5e-4; Fig. 2 Hypermutation in TEs that resembles the genome defense, Repeat-Induced Point mutation (RIP), has previously been observed in the LTR elements (copia-like and gypsylike elements) and Helitron transposons of M. lychnidis-dioicae Horns et al, 2012). Some genes that appeared similar to those necessary for RIP in Neurospora crassa (Cambareri et al, 1989;Selker et al, 1987) were found in the M. lychnidis-dioicae genome.…”