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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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Plot of McDonald–Kreitman test neutrality indices (NI) estimated from the combined pairwise species comparisons Zymoseptoria tritici–Z. pseudotritici, Z. tritici–Z. ardabiliae, and Z. pseudotritici–Z. ardabiliae. Values above zero (red) indicate diversifying selection, whereas values below zero (blue) indicate purifying selection. Significance values of P ≤ 0.01 are indicated with asterisks. (a) NIs for all 48 cell wall degrading enzymes organized according to CAZy families. (b) Combined NIs for multigene CAZy families. Detailed values are given in supplementary tables S3a and S3b, Supplementary Material online. CE, carbohydrate esterases; GH, glycoside hydrolases; PL, polysaccharide lyases.
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mst041-F2: Plot of McDonald–Kreitman test neutrality indices (NI) estimated from the combined pairwise species comparisons Zymoseptoria tritici–Z. pseudotritici, Z. tritici–Z. ardabiliae, and Z. pseudotritici–Z. ardabiliae. Values above zero (red) indicate diversifying selection, whereas values below zero (blue) indicate purifying selection. Significance values of P ≤ 0.01 are indicated with asterisks. (a) NIs for all 48 cell wall degrading enzymes organized according to CAZy families. (b) Combined NIs for multigene CAZy families. Detailed values are given in supplementary tables S3a and S3b, Supplementary Material online. CE, carbohydrate esterases; GH, glycoside hydrolases; PL, polysaccharide lyases.

Mentions: All PCWDEs showed nucleotide variability within and/or between species. Neutrality indices estimated from McDonald–Kreitman tests (MKTs) were significantly different from zero for 14 genes, suggesting that selection played an important role during the evolution of these PCWDEs (fig. 2; supplementary tables S3a and S3b, Supplementary Material online). With the exception of cellulases, significant purifying selection was indicated for 11 genes distributed over all classes. Accordingly, three genes were identified as being under positive selection, with one each attributed to the cutinases, cellulases, and hemicellulases.Fig. 2.


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)

Plot of McDonald–Kreitman test neutrality indices (NI) estimated from the combined pairwise species comparisons Zymoseptoria tritici–Z. pseudotritici, Z. tritici–Z. ardabiliae, and Z. pseudotritici–Z. ardabiliae. Values above zero (red) indicate diversifying selection, whereas values below zero (blue) indicate purifying selection. Significance values of P ≤ 0.01 are indicated with asterisks. (a) NIs for all 48 cell wall degrading enzymes organized according to CAZy families. (b) Combined NIs for multigene CAZy families. Detailed values are given in supplementary tables S3a and S3b, Supplementary Material online. CE, carbohydrate esterases; GH, glycoside hydrolases; PL, polysaccharide lyases.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

mst041-F2: Plot of McDonald–Kreitman test neutrality indices (NI) estimated from the combined pairwise species comparisons Zymoseptoria tritici–Z. pseudotritici, Z. tritici–Z. ardabiliae, and Z. pseudotritici–Z. ardabiliae. Values above zero (red) indicate diversifying selection, whereas values below zero (blue) indicate purifying selection. Significance values of P ≤ 0.01 are indicated with asterisks. (a) NIs for all 48 cell wall degrading enzymes organized according to CAZy families. (b) Combined NIs for multigene CAZy families. Detailed values are given in supplementary tables S3a and S3b, Supplementary Material online. CE, carbohydrate esterases; GH, glycoside hydrolases; PL, polysaccharide lyases.
Mentions: All PCWDEs showed nucleotide variability within and/or between species. Neutrality indices estimated from McDonald–Kreitman tests (MKTs) were significantly different from zero for 14 genes, suggesting that selection played an important role during the evolution of these PCWDEs (fig. 2; supplementary tables S3a and S3b, Supplementary Material online). With the exception of cellulases, significant purifying selection was indicated for 11 genes distributed over all classes. Accordingly, three genes were identified as being under positive selection, with one each attributed to the cutinases, cellulases, and hemicellulases.Fig. 2.

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