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

Amselem J, Lebrun MH, Quesneville H - BMC Genomics (2015)

Bottom Line: Both mechanisms require specific cytosine DNA Methyltransferases (RID1/Masc1) of the Dnmt1 superfamily.We identified fungal genomes containing large numbers of TEs with many C to T mutations associated with species-specific dinucleotide signatures.In particular, an RID1-dependent RIP mechanism was found only in Ascomycota.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR1164 URGI Research Unit in Genomics-Info, F-78026, Versailles, France. joelle.amselem@versailles.inra.fr.

ABSTRACT

Background: Transposable 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.

Results: We 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.

Conclusions: We 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.

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Functional annotation of 44 fungal Dnmt1 proteins and phylogenetic analysis of the cytosine-specific methyltransferase domain. (A) Phylogenetic analysis of 44 cytosine-specific methyltransferase domains (PTHR10629): Gray rectangles in 5B, including PF00145, PS00094, PS00095 et PR00105) from Dnmt1 fungal proteins and S. Pombe DNMT2, which was used as an outgroup. (B) Functional annotation of genes (white rectangle) with Interproscan (Cf Methods section). PTHR10629:SF10 is drawn on top of PTHR10629 (the coordinates are the same). Where PTHR10629 is not visible, it was overlapped by PF00145.
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Fig5: Functional annotation of 44 fungal Dnmt1 proteins and phylogenetic analysis of the cytosine-specific methyltransferase domain. (A) Phylogenetic analysis of 44 cytosine-specific methyltransferase domains (PTHR10629): Gray rectangles in 5B, including PF00145, PS00094, PS00095 et PR00105) from Dnmt1 fungal proteins and S. Pombe DNMT2, which was used as an outgroup. (B) Functional annotation of genes (white rectangle) with Interproscan (Cf Methods section). PTHR10629:SF10 is drawn on top of PTHR10629 (the coordinates are the same). Where PTHR10629 is not visible, it was overlapped by PF00145.

Mentions: We next addressed whether the differences in C to T mutation bias in TEs and their associated dinucleotide signatures among fungi could be explained by the presence/absence in these various species of different genes involved in this process. RIP and MIP require cytosine methyltransferases of the Dnmt1 family; therefore, we searched for 25 fungal genomes (included the 10 fungal genomes studied) for genes encoding Dnmt1 MTases. Forty-four proteins containing the cytosine specific methyltransferase Panther domain (PTHR10629) were recovered from these 25 genomes. This domain overlaps on both ends the C5-cytosine methyltransferase PFAM domain (PF00045), which is specific to the cytosine DNA MTase family (Figure 5B). Phylogenetic analysis of the PTHR10629 domain extracted from the 44 Dnmt1 protein sequences (Figure 5A) showed that these proteins clustered into two very distinct clades. The first clade (class I), contains proteins related to RID and Masc1 whereas the second clade (class II) contains proteins related to Dim2 and Masc2. This second clade is composed of two subclasses (IIA and IIB), corresponding to proteins related to either Masc2 or to Dim2, respectively. Interestingly, all the genomes with CpA or CpT dinucleotide signatures in TEs, had at least one gene coding for a protein of the Masc1/RID family (Dnmt1 class I, Figure 5A, Table 2). All these genomes belong to species of Ascomycota (Additional file 1). The three genomes that displayed only TEs with a CpG dinucleotide signature (Mvio, Mlar and Pgra) contained only one gene coding for a Dnmt1, a class IIA protein related to Masc2 (Figure 5A, Table 2). These three organisms belong to the Basidiomycota.Figure 5


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

Amselem J, Lebrun MH, Quesneville H - BMC Genomics (2015)

Functional annotation of 44 fungal Dnmt1 proteins and phylogenetic analysis of the cytosine-specific methyltransferase domain. (A) Phylogenetic analysis of 44 cytosine-specific methyltransferase domains (PTHR10629): Gray rectangles in 5B, including PF00145, PS00094, PS00095 et PR00105) from Dnmt1 fungal proteins and S. Pombe DNMT2, which was used as an outgroup. (B) Functional annotation of genes (white rectangle) with Interproscan (Cf Methods section). PTHR10629:SF10 is drawn on top of PTHR10629 (the coordinates are the same). Where PTHR10629 is not visible, it was overlapped by PF00145.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4352252&req=5

Fig5: Functional annotation of 44 fungal Dnmt1 proteins and phylogenetic analysis of the cytosine-specific methyltransferase domain. (A) Phylogenetic analysis of 44 cytosine-specific methyltransferase domains (PTHR10629): Gray rectangles in 5B, including PF00145, PS00094, PS00095 et PR00105) from Dnmt1 fungal proteins and S. Pombe DNMT2, which was used as an outgroup. (B) Functional annotation of genes (white rectangle) with Interproscan (Cf Methods section). PTHR10629:SF10 is drawn on top of PTHR10629 (the coordinates are the same). Where PTHR10629 is not visible, it was overlapped by PF00145.
Mentions: We next addressed whether the differences in C to T mutation bias in TEs and their associated dinucleotide signatures among fungi could be explained by the presence/absence in these various species of different genes involved in this process. RIP and MIP require cytosine methyltransferases of the Dnmt1 family; therefore, we searched for 25 fungal genomes (included the 10 fungal genomes studied) for genes encoding Dnmt1 MTases. Forty-four proteins containing the cytosine specific methyltransferase Panther domain (PTHR10629) were recovered from these 25 genomes. This domain overlaps on both ends the C5-cytosine methyltransferase PFAM domain (PF00045), which is specific to the cytosine DNA MTase family (Figure 5B). Phylogenetic analysis of the PTHR10629 domain extracted from the 44 Dnmt1 protein sequences (Figure 5A) showed that these proteins clustered into two very distinct clades. The first clade (class I), contains proteins related to RID and Masc1 whereas the second clade (class II) contains proteins related to Dim2 and Masc2. This second clade is composed of two subclasses (IIA and IIB), corresponding to proteins related to either Masc2 or to Dim2, respectively. Interestingly, all the genomes with CpA or CpT dinucleotide signatures in TEs, had at least one gene coding for a protein of the Masc1/RID family (Dnmt1 class I, Figure 5A, Table 2). All these genomes belong to species of Ascomycota (Additional file 1). The three genomes that displayed only TEs with a CpG dinucleotide signature (Mvio, Mlar and Pgra) contained only one gene coding for a Dnmt1, a class IIA protein related to Masc2 (Figure 5A, Table 2). These three organisms belong to the Basidiomycota.Figure 5

Bottom Line: Both mechanisms require specific cytosine DNA Methyltransferases (RID1/Masc1) of the Dnmt1 superfamily.We identified fungal genomes containing large numbers of TEs with many C to T mutations associated with species-specific dinucleotide signatures.In particular, an RID1-dependent RIP mechanism was found only in Ascomycota.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR1164 URGI Research Unit in Genomics-Info, F-78026, Versailles, France. joelle.amselem@versailles.inra.fr.

ABSTRACT

Background: Transposable 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.

Results: We 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.

Conclusions: We 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.

Show MeSH
Related in: MedlinePlus