Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes

Abstract

BackgroundTransposable Elements (TEs) are key components that shape the organization and evolution of genomes. Fungi have developed defense mechanisms against TE invasion such as RIP (Repeat-Induced Point mutation), MIP (Methylation Induced Premeiotically) and Quelling (RNA interference). RIP inactivates repeated sequences by promoting Cytosine to Thymine mutations, whereas MIP only methylates TEs at C residues. Both mechanisms require specific cytosine DNA Methyltransferases (RID1/Masc1) of the Dnmt1 superfamily.ResultsWe annotated TE sequences from 10 fungal genomes with different TE content (1-70%). We then used these TE sequences to carry out a genome-wide analysis of C to T mutations biases. Genomes from either Ascomycota or Basidiomycota that were massively invaded by TEs (Blumeria, Melampsora, Puccinia) were characterized by a low frequency of C to T mutation bias (10-20%), whereas other genomes displayed intermediate to high frequencies (25-75%). We identified several dinucleotide signatures at these C to T mutation sites (CpA, CpT, and CpG). Phylogenomic analysis of fungal Dnmt1 MTases revealed a previously unreported association between these dinucleotide signatures and the presence/absence of sub-classes of Dnmt1.ConclusionsWe identified fungal genomes containing large numbers of TEs with many C to T mutations associated with species-specific dinucleotide signatures. This bias suggests that a basic defense mechanism against TE invasion similar to RIP is widespread in fungi, although the efficiency and specificity of this mechanism differs between species. Our analysis revealed that dinucleotide signatures are associated with the presence/absence of specific Dnmt1 subfamilies. In particular, an RID1-dependent RIP mechanism was found only in Ascomycota.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1347-1) contains supplementary material, which is available to authorized users.

The botrydial biosynthetic gene cluster of Botrytis cinerea displays a bipartite genomic structure and is positively regulated by the putative Zn(II)2Cys6 transcription factor BcBot6

“…Particularly, the area containing Bcbot1-Bcbot5 genes is 47.26% G + C-rich whereas upstream and downstream gene-less regions only contain 11.86 and 13.09% of G + C, respectively. In many fungi including B. cinerea, it is well documented that A + T-rich regions may result from a pre-meiotic genome defense mechanism named RepeatInduced Point mutation (RIP) that silences repeated sequences by mutating C to T consequently increasing the A + T content (Amselem et al, 2015;Hane et al, 2015). We thereby tested the hypothesis that the presence of A + T-rich regions surrounding the BOT gene cluster might originate from transposable elements Kan et al, 2016) which allowed to detect the genes located upstream and downstream from the five previously identified Bcbot genes (Pinedo et al, 2008).…”

“…fr/tools/REPET; Amselem et al, 2015). The TEdenovo pipeline (Flutre et al, 2011) was used to detect repeated elements in the genome and to provide a consensus sequence for each family.…”

Population diversity and genomics of the fungal pathogen of canola Leptosphaeria maculans

“…Class I retrotransposons and Class II DNA transposons (Amselem et al, 2015). They are known to play a role in modifying the genomic structure of an organism via genome size expansion, gene duplications, chromosomal rearrangements, inactivation of genes and gene loss (Amselem et al, 2015).…”

“…They are known to play a role in modifying the genomic structure of an organism via genome size expansion, gene duplications, chromosomal rearrangements, inactivation of genes and gene loss (Amselem et al, 2015). In blackleg, 80% of detected TEs belong to the Class I category and they occur as clustered blocks, the majority of which are truncated mosaics (Rouxel et al, 2011).…”

“…TEs are affected by RIP mutations and their mosaics are mainly found in AT-rich regions of the genome. The genomes of other pathogens such as Phytophthora infestans and Blumeria graminis have been known to undergo significant expansion due to the invasion of TEs and absence of mechanism that keep TE activity in check (Amselem et al, 2015). In L. maculans however, genome expansion via TE invasion has been controlled due to the activity of RIP that renders their transposition mechanism useless (Grandaubert et al, 2014b).…”