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Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations.

Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciuffetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GH, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, Turgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent MH, Howlett BJ - Nat Commun (2011)

Bottom Line: Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification.The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism.This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.

View Article: PubMed Central - PubMed

Affiliation: INRA-Bioger, UR1290, Avenue Lucien Brétignières, BP 01, Thiverval-Grignon F-78850, France. rouxel@versailles.inra.fr

ABSTRACT
Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.

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Phylogenetic relationships between Dothideomycetes and an example of microsynteny between related species.(a) An example of microsynteny between L. maculans and closely related Dothideomycetes, P. nodorum, C. heterostrophus and P. tritici-repentis, showing the integration of an AT-rich genomic region (grey boxes) between two orthologous genes encoding for fungal transcription factors (red and green arrows) of the three other species, along with generation of one novel small-secreted protein-encoding gene (blue arrow) in L. maculans only. Grey arrow, P. nodorum predicted gene. The ID of each gene in the corresponding genome sequence is indicated. The intergenic distance (expressed in kb) is shown. (b) A phylogenetic tree and estimated time divergences of major lineages in Ascomycota with a selection of plant pathogenic lineages in Dothideomycetes. The phylogenetic analysis was performed using RaxML44 and the chronogram, calibrated using recent data from the literature and fossil dates, produced using r8s (ref. 45). Classes outside of the Dothideomycetes were collapsed in TreeDyn, except for Sordariomycetes where the order Hypocreales represented an important calibration point. The blue vertical lines correlate with divergence times when the root of the tree was fixed at 500 MYA, whereas the green lines of the tree represent a fixed root of 650 MYA. The range of dates for the emergence of Dothideomycetes and Pleosporineae are highlighted with stippled lines. Thickened branches on the tree represents nodes that had more than 70% bootstrap values in a RAxML run. Species with genome data are marked with a DNA logo.
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f1: Phylogenetic relationships between Dothideomycetes and an example of microsynteny between related species.(a) An example of microsynteny between L. maculans and closely related Dothideomycetes, P. nodorum, C. heterostrophus and P. tritici-repentis, showing the integration of an AT-rich genomic region (grey boxes) between two orthologous genes encoding for fungal transcription factors (red and green arrows) of the three other species, along with generation of one novel small-secreted protein-encoding gene (blue arrow) in L. maculans only. Grey arrow, P. nodorum predicted gene. The ID of each gene in the corresponding genome sequence is indicated. The intergenic distance (expressed in kb) is shown. (b) A phylogenetic tree and estimated time divergences of major lineages in Ascomycota with a selection of plant pathogenic lineages in Dothideomycetes. The phylogenetic analysis was performed using RaxML44 and the chronogram, calibrated using recent data from the literature and fossil dates, produced using r8s (ref. 45). Classes outside of the Dothideomycetes were collapsed in TreeDyn, except for Sordariomycetes where the order Hypocreales represented an important calibration point. The blue vertical lines correlate with divergence times when the root of the tree was fixed at 500 MYA, whereas the green lines of the tree represent a fixed root of 650 MYA. The range of dates for the emergence of Dothideomycetes and Pleosporineae are highlighted with stippled lines. Thickened branches on the tree represents nodes that had more than 70% bootstrap values in a RAxML run. Species with genome data are marked with a DNA logo.

Mentions: The haploid genome of strain v23.1.3 of L. maculans 'brassicae' was sequenced using a whole-genome shotgun strategy. This fungus is closely related to Phaeosphaeria (Stagonospora) nodorum, Pyrenophora tritici-repentis and Cochliobolus heterostrophus, as seen in the phylogeny based on sequence analysis of a range of genes (Supplementary Table S1; Fig. 1). The genome assembly had a total size of 45.12 Mb, scaffolded into 76 SuperContigs (SCs; 30 large SCs >143 kb; Tables 1 and 2; Supplementary Table S2). The correspondence of SCs to chromosomes was inferred by a combination of approaches (Fig. 2; Supplementary Figs S1 and S2). Conglomerated data are consistent with the presence of 17 or 18 chromosomes, ten of which correspond to single SCs (Supplementary Fig. S1; Supplementary Table S2).


Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations.

Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciuffetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GH, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, Turgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent MH, Howlett BJ - Nat Commun (2011)

Phylogenetic relationships between Dothideomycetes and an example of microsynteny between related species.(a) An example of microsynteny between L. maculans and closely related Dothideomycetes, P. nodorum, C. heterostrophus and P. tritici-repentis, showing the integration of an AT-rich genomic region (grey boxes) between two orthologous genes encoding for fungal transcription factors (red and green arrows) of the three other species, along with generation of one novel small-secreted protein-encoding gene (blue arrow) in L. maculans only. Grey arrow, P. nodorum predicted gene. The ID of each gene in the corresponding genome sequence is indicated. The intergenic distance (expressed in kb) is shown. (b) A phylogenetic tree and estimated time divergences of major lineages in Ascomycota with a selection of plant pathogenic lineages in Dothideomycetes. The phylogenetic analysis was performed using RaxML44 and the chronogram, calibrated using recent data from the literature and fossil dates, produced using r8s (ref. 45). Classes outside of the Dothideomycetes were collapsed in TreeDyn, except for Sordariomycetes where the order Hypocreales represented an important calibration point. The blue vertical lines correlate with divergence times when the root of the tree was fixed at 500 MYA, whereas the green lines of the tree represent a fixed root of 650 MYA. The range of dates for the emergence of Dothideomycetes and Pleosporineae are highlighted with stippled lines. Thickened branches on the tree represents nodes that had more than 70% bootstrap values in a RAxML run. Species with genome data are marked with a DNA logo.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105345&req=5

f1: Phylogenetic relationships between Dothideomycetes and an example of microsynteny between related species.(a) An example of microsynteny between L. maculans and closely related Dothideomycetes, P. nodorum, C. heterostrophus and P. tritici-repentis, showing the integration of an AT-rich genomic region (grey boxes) between two orthologous genes encoding for fungal transcription factors (red and green arrows) of the three other species, along with generation of one novel small-secreted protein-encoding gene (blue arrow) in L. maculans only. Grey arrow, P. nodorum predicted gene. The ID of each gene in the corresponding genome sequence is indicated. The intergenic distance (expressed in kb) is shown. (b) A phylogenetic tree and estimated time divergences of major lineages in Ascomycota with a selection of plant pathogenic lineages in Dothideomycetes. The phylogenetic analysis was performed using RaxML44 and the chronogram, calibrated using recent data from the literature and fossil dates, produced using r8s (ref. 45). Classes outside of the Dothideomycetes were collapsed in TreeDyn, except for Sordariomycetes where the order Hypocreales represented an important calibration point. The blue vertical lines correlate with divergence times when the root of the tree was fixed at 500 MYA, whereas the green lines of the tree represent a fixed root of 650 MYA. The range of dates for the emergence of Dothideomycetes and Pleosporineae are highlighted with stippled lines. Thickened branches on the tree represents nodes that had more than 70% bootstrap values in a RAxML run. Species with genome data are marked with a DNA logo.
Mentions: The haploid genome of strain v23.1.3 of L. maculans 'brassicae' was sequenced using a whole-genome shotgun strategy. This fungus is closely related to Phaeosphaeria (Stagonospora) nodorum, Pyrenophora tritici-repentis and Cochliobolus heterostrophus, as seen in the phylogeny based on sequence analysis of a range of genes (Supplementary Table S1; Fig. 1). The genome assembly had a total size of 45.12 Mb, scaffolded into 76 SuperContigs (SCs; 30 large SCs >143 kb; Tables 1 and 2; Supplementary Table S2). The correspondence of SCs to chromosomes was inferred by a combination of approaches (Fig. 2; Supplementary Figs S1 and S2). Conglomerated data are consistent with the presence of 17 or 18 chromosomes, ten of which correspond to single SCs (Supplementary Fig. S1; Supplementary Table S2).

Bottom Line: Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification.The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism.This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.

View Article: PubMed Central - PubMed

Affiliation: INRA-Bioger, UR1290, Avenue Lucien Brétignières, BP 01, Thiverval-Grignon F-78850, France. rouxel@versailles.inra.fr

ABSTRACT
Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.

Show MeSH