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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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Repeat-induced point (RIP) mutation in ribosomal DNA of L. maculans shown as RIPCAL output.(a) Schematic representation of the rDNA unit in L. maculans (ITS, internal transcribed spacers; IGS, intergenic spacer); (b) a schematic multiple alignment of the 7.8 kb 'complete' ribosomal DNA (rDNA) units occurring in SuperContigs 2 and 19. Polymorphic nucleotides are coloured as a function of the type of RIP mutation observed, with black, invariant nucleotide; red, CpA  TpA or TpG  TpA mutations; dark blue, CpC  TpC or GpG  GpA mutations; pale blue, CpT  TpT or ApG  ApA mutations; green, CpG  TpG or CpG  CpA mutations; (c) RIP mutation frequency plot over a rolling sequence window, corresponding to the multiple alignment directly above. Nucleotide polymorphisms (against the alignment consensus, which is also the highest GC-content sequence) mostly correspond to CpA  TpA or TpG  TpA (red curve) and CpG  TpG or CpG  CpA (green curve).
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f3: Repeat-induced point (RIP) mutation in ribosomal DNA of L. maculans shown as RIPCAL output.(a) Schematic representation of the rDNA unit in L. maculans (ITS, internal transcribed spacers; IGS, intergenic spacer); (b) a schematic multiple alignment of the 7.8 kb 'complete' ribosomal DNA (rDNA) units occurring in SuperContigs 2 and 19. Polymorphic nucleotides are coloured as a function of the type of RIP mutation observed, with black, invariant nucleotide; red, CpA TpA or TpG TpA mutations; dark blue, CpC TpC or GpG GpA mutations; pale blue, CpT TpT or ApG ApA mutations; green, CpG TpG or CpG CpA mutations; (c) RIP mutation frequency plot over a rolling sequence window, corresponding to the multiple alignment directly above. Nucleotide polymorphisms (against the alignment consensus, which is also the highest GC-content sequence) mostly correspond to CpA TpA or TpG TpA (red curve) and CpG TpG or CpG CpA (green curve).

Mentions: In eukaryotes, the ribosomal DNA (rDNA) comprises a multigene family organized as large arrays of tandem repeats. The core unit is a single transcription unit that includes the 18S or Small Subunit, 5.8S, and 28S or Large Subunit separated by internal transcribed spacers (ITS1 and ITS2). Each transcription unit is separated by the Intergenic Spacer (Fig. 3a). Although essential duplicated regions would be expected to be protected from RIP mutations, the rDNA repeats in L. maculans are in part affected by RIP (Fig. 3b,c, Supplementary Fig. S10). The number of rDNA repeats ranges between 56 and 225 in different L. maculans isolates23. The assembly of strain v23.1.3 has >150 repeats, only two of which are highly similar (99.6% identity) and are not affected by RIP. Fifty complete rDNA units and 107 incomplete units are present, and most of them are on extreme ends of SC2 and SC19, which are not complete chromosomes. Many of these repeats are severely affected by RIP (Fig. 3, Supplementary Fig. S10). Selker24 has suggested that rDNA repeats in the nucleolus organizer region are protected from RIP. Our data indicate that this is not the case in L. maculans, at least for a part of the array of tandem repeats.


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)

Repeat-induced point (RIP) mutation in ribosomal DNA of L. maculans shown as RIPCAL output.(a) Schematic representation of the rDNA unit in L. maculans (ITS, internal transcribed spacers; IGS, intergenic spacer); (b) a schematic multiple alignment of the 7.8 kb 'complete' ribosomal DNA (rDNA) units occurring in SuperContigs 2 and 19. Polymorphic nucleotides are coloured as a function of the type of RIP mutation observed, with black, invariant nucleotide; red, CpA  TpA or TpG  TpA mutations; dark blue, CpC  TpC or GpG  GpA mutations; pale blue, CpT  TpT or ApG  ApA mutations; green, CpG  TpG or CpG  CpA mutations; (c) RIP mutation frequency plot over a rolling sequence window, corresponding to the multiple alignment directly above. Nucleotide polymorphisms (against the alignment consensus, which is also the highest GC-content sequence) mostly correspond to CpA  TpA or TpG  TpA (red curve) and CpG  TpG or CpG  CpA (green curve).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Repeat-induced point (RIP) mutation in ribosomal DNA of L. maculans shown as RIPCAL output.(a) Schematic representation of the rDNA unit in L. maculans (ITS, internal transcribed spacers; IGS, intergenic spacer); (b) a schematic multiple alignment of the 7.8 kb 'complete' ribosomal DNA (rDNA) units occurring in SuperContigs 2 and 19. Polymorphic nucleotides are coloured as a function of the type of RIP mutation observed, with black, invariant nucleotide; red, CpA TpA or TpG TpA mutations; dark blue, CpC TpC or GpG GpA mutations; pale blue, CpT TpT or ApG ApA mutations; green, CpG TpG or CpG CpA mutations; (c) RIP mutation frequency plot over a rolling sequence window, corresponding to the multiple alignment directly above. Nucleotide polymorphisms (against the alignment consensus, which is also the highest GC-content sequence) mostly correspond to CpA TpA or TpG TpA (red curve) and CpG TpG or CpG CpA (green curve).
Mentions: In eukaryotes, the ribosomal DNA (rDNA) comprises a multigene family organized as large arrays of tandem repeats. The core unit is a single transcription unit that includes the 18S or Small Subunit, 5.8S, and 28S or Large Subunit separated by internal transcribed spacers (ITS1 and ITS2). Each transcription unit is separated by the Intergenic Spacer (Fig. 3a). Although essential duplicated regions would be expected to be protected from RIP mutations, the rDNA repeats in L. maculans are in part affected by RIP (Fig. 3b,c, Supplementary Fig. S10). The number of rDNA repeats ranges between 56 and 225 in different L. maculans isolates23. The assembly of strain v23.1.3 has >150 repeats, only two of which are highly similar (99.6% identity) and are not affected by RIP. Fifty complete rDNA units and 107 incomplete units are present, and most of them are on extreme ends of SC2 and SC19, which are not complete chromosomes. Many of these repeats are severely affected by RIP (Fig. 3, Supplementary Fig. S10). Selker24 has suggested that rDNA repeats in the nucleolus organizer region are protected from RIP. Our data indicate that this is not the case in L. maculans, at least for a part of the array of tandem repeats.

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