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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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Main features of the L. maculans genome as exemplified by chromosome 5 SuperContig 1.(a) Transposable elements (TEs) distribution and gene density along the supercontig. TE density is drawn in green and gene density is in blue. (b) Location of SSPs (small-secreted protein encoding genes). Blue arrowheads, SSP in AT-blocks, corresponding to TE-rich regions in a; red arrowheads, SSP in GC-blocks, corresponding to gene-rich genome regions in a. (c) GC content along the SC showing alternating GC-equilibrated and AT-rich regions, with location of a polyketide synthase-encoding gene, PKS4. (d) Genetic (upper part, expressed in centiMorgan—cM) to physical (expressed in kb) distance relationship as a function of the isochore-like structure. Lower part: physical location of genetic markers. Upper part of the panel: genetic map using MapMaker/Exp 3.0 with parameters set at likelihood ratio value >3.0 and minimum distance=20 cM. Only markers drawn from the sequence data are represented.
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f2: Main features of the L. maculans genome as exemplified by chromosome 5 SuperContig 1.(a) Transposable elements (TEs) distribution and gene density along the supercontig. TE density is drawn in green and gene density is in blue. (b) Location of SSPs (small-secreted protein encoding genes). Blue arrowheads, SSP in AT-blocks, corresponding to TE-rich regions in a; red arrowheads, SSP in GC-blocks, corresponding to gene-rich genome regions in a. (c) GC content along the SC showing alternating GC-equilibrated and AT-rich regions, with location of a polyketide synthase-encoding gene, PKS4. (d) Genetic (upper part, expressed in centiMorgan—cM) to physical (expressed in kb) distance relationship as a function of the isochore-like structure. Lower part: physical location of genetic markers. Upper part of the panel: genetic map using MapMaker/Exp 3.0 with parameters set at likelihood ratio value >3.0 and minimum distance=20 cM. Only markers drawn from the sequence data are represented.

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)

Main features of the L. maculans genome as exemplified by chromosome 5 SuperContig 1.(a) Transposable elements (TEs) distribution and gene density along the supercontig. TE density is drawn in green and gene density is in blue. (b) Location of SSPs (small-secreted protein encoding genes). Blue arrowheads, SSP in AT-blocks, corresponding to TE-rich regions in a; red arrowheads, SSP in GC-blocks, corresponding to gene-rich genome regions in a. (c) GC content along the SC showing alternating GC-equilibrated and AT-rich regions, with location of a polyketide synthase-encoding gene, PKS4. (d) Genetic (upper part, expressed in centiMorgan—cM) to physical (expressed in kb) distance relationship as a function of the isochore-like structure. Lower part: physical location of genetic markers. Upper part of the panel: genetic map using MapMaker/Exp 3.0 with parameters set at likelihood ratio value >3.0 and minimum distance=20 cM. Only markers drawn from the sequence data are represented.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Main features of the L. maculans genome as exemplified by chromosome 5 SuperContig 1.(a) Transposable elements (TEs) distribution and gene density along the supercontig. TE density is drawn in green and gene density is in blue. (b) Location of SSPs (small-secreted protein encoding genes). Blue arrowheads, SSP in AT-blocks, corresponding to TE-rich regions in a; red arrowheads, SSP in GC-blocks, corresponding to gene-rich genome regions in a. (c) GC content along the SC showing alternating GC-equilibrated and AT-rich regions, with location of a polyketide synthase-encoding gene, PKS4. (d) Genetic (upper part, expressed in centiMorgan—cM) to physical (expressed in kb) distance relationship as a function of the isochore-like structure. Lower part: physical location of genetic markers. Upper part of the panel: genetic map using MapMaker/Exp 3.0 with parameters set at likelihood ratio value >3.0 and minimum distance=20 cM. Only markers drawn from the sequence data are represented.
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
Related in: MedlinePlus