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Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen.

Brunner PC, Torriani SF, Croll D, Stukenbrock EH, McDonald BA - Mol. Biol. Evol. (2013)

Bottom Line: We found widespread differential transcription among different members of the same gene family, challenging the idea of functional redundancy and suggesting instead that specialized enzymatic activity occurs during different stages of the pathogen life cycle.We also find that natural selection has significantly affected at least 19 of the 48 identified PCWDEs.However, six genes showed diversifying selection that could be attributed to either host adaptation or host evasion.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Systems Science, Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland. patrick.brunner@usys.ethz.ch

ABSTRACT
Zymoseptoria tritici is an important fungal pathogen on wheat that originated in the Fertile Crescent. Its closely related sister species Z. pseudotritici and Z. ardabiliae infect wild grasses in the same region. This recently emerged host-pathogen system provides a rare opportunity to investigate the evolutionary processes shaping the genome of an emerging pathogen. Here, we investigate genetic signatures in plant cell wall degrading enzymes (PCWDEs) that are likely affected by or driving coevolution in plant-pathogen systems. We hypothesize four main evolutionary scenarios and combine comparative genomics, transcriptomics, and selection analyses to assign the majority of PCWDEs in Z. tritici to one of these scenarios. We found widespread differential transcription among different members of the same gene family, challenging the idea of functional redundancy and suggesting instead that specialized enzymatic activity occurs during different stages of the pathogen life cycle. We also find that natural selection has significantly affected at least 19 of the 48 identified PCWDEs. The majority of genes showed signatures of purifying selection, typical for the scenario of conserved substrate optimization. However, six genes showed diversifying selection that could be attributed to either host adaptation or host evasion. This study provides a powerful framework to better understand the roles played by different members of multigene families and to determine which genes are the most appropriate targets for wet laboratory experimentation, for example, to elucidate enzymatic function during relevant phases of a pathogen's life cycle.

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Likelihood ratio tests to detect selection heterogeneity across the phylogeny of Zymoseptoria tritici against its ancestors for all 48 cell wall degrading enzymes. (a) Phylogeny and models used to assess heterogeneity in dN/dS. Models M2–M5 assume heterogeneity on different levels and are compared against the -model M1 assuming a constant dN/dS value. (b) Gene frequencies of significantly higher dN/dS ratios (red) or significantly lower dN/dS ratios (blue) for Z. tritici at P ≤ 0.01. Nonsignificant selection heterogeneity is indicated in yellow. Detailed values are given in supplementary table S4, Supplementary Material online.
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mst041-F3: Likelihood ratio tests to detect selection heterogeneity across the phylogeny of Zymoseptoria tritici against its ancestors for all 48 cell wall degrading enzymes. (a) Phylogeny and models used to assess heterogeneity in dN/dS. Models M2–M5 assume heterogeneity on different levels and are compared against the -model M1 assuming a constant dN/dS value. (b) Gene frequencies of significantly higher dN/dS ratios (red) or significantly lower dN/dS ratios (blue) for Z. tritici at P ≤ 0.01. Nonsignificant selection heterogeneity is indicated in yellow. Detailed values are given in supplementary table S4, Supplementary Material online.

Mentions: We used phylogenetic analyses to assess whether significant differences in selection pressure, as measured by dN/dS ratios, were operating on the PCWDEs during the evolution of Z. tritici. Models 1 and 2, which assume the same dN/dS ratios for Z. tritici and its ancestors (i.e., no selection heterogeneity), were the best models for 36 genes. However, 12 genes showed significant heterogeneity in dN/dS at P ≤ 0.01, supporting our hypothesis that changing selection pressure has affected the evolution of PCWDEs (fig. 3; supplementary table S4, Supplementary Material online). Of these, eight genes showed significantly lower dN/dS, suggestive of an increase in purifying selection, and four genes showed a significantly higher dN/dS, suggestive of an increase in diversifying selection in Z. tritici, for example, due to the new environment/host species (supplementary table S4, Supplementary Material online). A detailed summary of the main findings for each class of PCWDE is provided as supplementary results, Supplementary Material online.Fig. 3.


Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen.

Brunner PC, Torriani SF, Croll D, Stukenbrock EH, McDonald BA - Mol. Biol. Evol. (2013)

Likelihood ratio tests to detect selection heterogeneity across the phylogeny of Zymoseptoria tritici against its ancestors for all 48 cell wall degrading enzymes. (a) Phylogeny and models used to assess heterogeneity in dN/dS. Models M2–M5 assume heterogeneity on different levels and are compared against the -model M1 assuming a constant dN/dS value. (b) Gene frequencies of significantly higher dN/dS ratios (red) or significantly lower dN/dS ratios (blue) for Z. tritici at P ≤ 0.01. Nonsignificant selection heterogeneity is indicated in yellow. Detailed values are given in supplementary table S4, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3649673&req=5

mst041-F3: Likelihood ratio tests to detect selection heterogeneity across the phylogeny of Zymoseptoria tritici against its ancestors for all 48 cell wall degrading enzymes. (a) Phylogeny and models used to assess heterogeneity in dN/dS. Models M2–M5 assume heterogeneity on different levels and are compared against the -model M1 assuming a constant dN/dS value. (b) Gene frequencies of significantly higher dN/dS ratios (red) or significantly lower dN/dS ratios (blue) for Z. tritici at P ≤ 0.01. Nonsignificant selection heterogeneity is indicated in yellow. Detailed values are given in supplementary table S4, Supplementary Material online.
Mentions: We used phylogenetic analyses to assess whether significant differences in selection pressure, as measured by dN/dS ratios, were operating on the PCWDEs during the evolution of Z. tritici. Models 1 and 2, which assume the same dN/dS ratios for Z. tritici and its ancestors (i.e., no selection heterogeneity), were the best models for 36 genes. However, 12 genes showed significant heterogeneity in dN/dS at P ≤ 0.01, supporting our hypothesis that changing selection pressure has affected the evolution of PCWDEs (fig. 3; supplementary table S4, Supplementary Material online). Of these, eight genes showed significantly lower dN/dS, suggestive of an increase in purifying selection, and four genes showed a significantly higher dN/dS, suggestive of an increase in diversifying selection in Z. tritici, for example, due to the new environment/host species (supplementary table S4, Supplementary Material online). A detailed summary of the main findings for each class of PCWDE is provided as supplementary results, Supplementary Material online.Fig. 3.

Bottom Line: We found widespread differential transcription among different members of the same gene family, challenging the idea of functional redundancy and suggesting instead that specialized enzymatic activity occurs during different stages of the pathogen life cycle.We also find that natural selection has significantly affected at least 19 of the 48 identified PCWDEs.However, six genes showed diversifying selection that could be attributed to either host adaptation or host evasion.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Systems Science, Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland. patrick.brunner@usys.ethz.ch

ABSTRACT
Zymoseptoria tritici is an important fungal pathogen on wheat that originated in the Fertile Crescent. Its closely related sister species Z. pseudotritici and Z. ardabiliae infect wild grasses in the same region. This recently emerged host-pathogen system provides a rare opportunity to investigate the evolutionary processes shaping the genome of an emerging pathogen. Here, we investigate genetic signatures in plant cell wall degrading enzymes (PCWDEs) that are likely affected by or driving coevolution in plant-pathogen systems. We hypothesize four main evolutionary scenarios and combine comparative genomics, transcriptomics, and selection analyses to assign the majority of PCWDEs in Z. tritici to one of these scenarios. We found widespread differential transcription among different members of the same gene family, challenging the idea of functional redundancy and suggesting instead that specialized enzymatic activity occurs during different stages of the pathogen life cycle. We also find that natural selection has significantly affected at least 19 of the 48 identified PCWDEs. The majority of genes showed signatures of purifying selection, typical for the scenario of conserved substrate optimization. However, six genes showed diversifying selection that could be attributed to either host adaptation or host evasion. This study provides a powerful framework to better understand the roles played by different members of multigene families and to determine which genes are the most appropriate targets for wet laboratory experimentation, for example, to elucidate enzymatic function during relevant phases of a pathogen's life cycle.

Show MeSH