Limits...
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.

Show MeSH

Related in: MedlinePlus

Dynamics of transposable elements in the L. maculans genome.A phylogenetic analysis was used to retrace the evolutionary history of each transposable element (TE) family after elimination of mutations due to repeat-induced point mutations. Terminal fork branch lengths were assumed to correspond to an evolutionary distance used to estimate the age of the last transposition activity. The divergence values were converted to estimated divergence time using a substitution rate of 1.05×10−9 substitution per location per year5253 (expressed as 'million years ago' MYA). (a) Box plot graph of divergence times. The red line represents the median value; the boxes include values between the first and the third quartile of the distribution; squares and circles, first and ninth decile, respectively. (b) Kernel density of divergence plots. A R-script was written to plot a histogram of the terminal fork branch length with kernel density estimate for each family.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3105345&req=5

f4: Dynamics of transposable elements in the L. maculans genome.A phylogenetic analysis was used to retrace the evolutionary history of each transposable element (TE) family after elimination of mutations due to repeat-induced point mutations. Terminal fork branch lengths were assumed to correspond to an evolutionary distance used to estimate the age of the last transposition activity. The divergence values were converted to estimated divergence time using a substitution rate of 1.05×10−9 substitution per location per year5253 (expressed as 'million years ago' MYA). (a) Box plot graph of divergence times. The red line represents the median value; the boxes include values between the first and the third quartile of the distribution; squares and circles, first and ninth decile, respectively. (b) Kernel density of divergence plots. A R-script was written to plot a histogram of the terminal fork branch length with kernel density estimate for each family.

Mentions: A range of 278–320 MYA is estimated for the origin of the Dothideomycetes with the crown radiation of the class during the Permian (251–289 MYA; Fig. 1b). The origins of the plant pathogenic Pleosporineae is determined at 97–112 MYA, placing it in the Cretaceous at a time when flowering plants were beginning to become widespread and eudicots were emerging, during the late Cretaceous and Paleocene. Leptosphaeria likely diverged from the other species analysed between 50 and 57 MYA (Fig. 1b). Phylogenetic analyses suggest three main features of genome invasion by TEs: transposition bursts mostly after separation of L. maculans from other species of suborder Pleosporineae as indicated by a 'recent' divergence of the TE families, estimated to 4–20 MYA (Fig. 4a); a single or few wave(s) of massive transposition(s) followed by a 'rapid' decay, with some cases like DTM_Sahana where divergence between copies is extremely low; and no on-going waves of genome invasion by TEs (Fig. 4b). Like other organisms with a high density of TEs, the L. maculans genome exhibits 'nesting', where repeats occur within previously inserted TEs. In this fungus, TEs are commonly invaded by other TEs generating a complex 'nesting network'. Eighty-five % of these cases correspond to TEs invading one other TE (primary nesting relationship). Most of the retrotransposon families investigated can invade or be invaded to similar extents (Supplementary Table S8). They also can invade TEs from the same family (self-nests), but usually at a very low frequency compared with invasion of retrotransposons from other families. In contrast, the DNA transposons are more commonly invaded (23.3% of the cases) than acting as invaders (3.5% of the cases; Supplementary Table S8). In accordance with overlapping divergence time estimates (Figs 1b and 4), these data indicate periods of overlapping transpositional activity for the long terminal repeats retrotransposons that form the major part of AT-blocks. In such a scenario, the later insertions would be preferentially tolerated in existing decayed transposons. These TEs, having undergone RIP in their turn, would initiate a positive reinforcement loop that would create large AT-rich and gene-poor blocks of homogeneous nucleotide composition.


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)

Dynamics of transposable elements in the L. maculans genome.A phylogenetic analysis was used to retrace the evolutionary history of each transposable element (TE) family after elimination of mutations due to repeat-induced point mutations. Terminal fork branch lengths were assumed to correspond to an evolutionary distance used to estimate the age of the last transposition activity. The divergence values were converted to estimated divergence time using a substitution rate of 1.05×10−9 substitution per location per year5253 (expressed as 'million years ago' MYA). (a) Box plot graph of divergence times. The red line represents the median value; the boxes include values between the first and the third quartile of the distribution; squares and circles, first and ninth decile, respectively. (b) Kernel density of divergence plots. A R-script was written to plot a histogram of the terminal fork branch length with kernel density estimate for each family.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Dynamics of transposable elements in the L. maculans genome.A phylogenetic analysis was used to retrace the evolutionary history of each transposable element (TE) family after elimination of mutations due to repeat-induced point mutations. Terminal fork branch lengths were assumed to correspond to an evolutionary distance used to estimate the age of the last transposition activity. The divergence values were converted to estimated divergence time using a substitution rate of 1.05×10−9 substitution per location per year5253 (expressed as 'million years ago' MYA). (a) Box plot graph of divergence times. The red line represents the median value; the boxes include values between the first and the third quartile of the distribution; squares and circles, first and ninth decile, respectively. (b) Kernel density of divergence plots. A R-script was written to plot a histogram of the terminal fork branch length with kernel density estimate for each family.
Mentions: A range of 278–320 MYA is estimated for the origin of the Dothideomycetes with the crown radiation of the class during the Permian (251–289 MYA; Fig. 1b). The origins of the plant pathogenic Pleosporineae is determined at 97–112 MYA, placing it in the Cretaceous at a time when flowering plants were beginning to become widespread and eudicots were emerging, during the late Cretaceous and Paleocene. Leptosphaeria likely diverged from the other species analysed between 50 and 57 MYA (Fig. 1b). Phylogenetic analyses suggest three main features of genome invasion by TEs: transposition bursts mostly after separation of L. maculans from other species of suborder Pleosporineae as indicated by a 'recent' divergence of the TE families, estimated to 4–20 MYA (Fig. 4a); a single or few wave(s) of massive transposition(s) followed by a 'rapid' decay, with some cases like DTM_Sahana where divergence between copies is extremely low; and no on-going waves of genome invasion by TEs (Fig. 4b). Like other organisms with a high density of TEs, the L. maculans genome exhibits 'nesting', where repeats occur within previously inserted TEs. In this fungus, TEs are commonly invaded by other TEs generating a complex 'nesting network'. Eighty-five % of these cases correspond to TEs invading one other TE (primary nesting relationship). Most of the retrotransposon families investigated can invade or be invaded to similar extents (Supplementary Table S8). They also can invade TEs from the same family (self-nests), but usually at a very low frequency compared with invasion of retrotransposons from other families. In contrast, the DNA transposons are more commonly invaded (23.3% of the cases) than acting as invaders (3.5% of the cases; Supplementary Table S8). In accordance with overlapping divergence time estimates (Figs 1b and 4), these data indicate periods of overlapping transpositional activity for the long terminal repeats retrotransposons that form the major part of AT-blocks. In such a scenario, the later insertions would be preferentially tolerated in existing decayed transposons. These TEs, having undergone RIP in their turn, would initiate a positive reinforcement loop that would create large AT-rich and gene-poor blocks of homogeneous nucleotide composition.

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