Limits...
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.

Show MeSH
Standardized transcription values (RPKM) from RNA-Seq experiments in Zymoseptoria tritici indicate differential in planta expression for cutinase genes during the biotrophic, necrotrophic, and saprotrophic life cycle stages. The gene expression bars represent the average from three biological replicates and error bars are one standard deviation from the mean; dpi, days post-inoculation. Detailed values for all cell wall degrading enzymes are given in supplementary table S2, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3649673&req=5

mst041-F1: Standardized transcription values (RPKM) from RNA-Seq experiments in Zymoseptoria tritici indicate differential in planta expression for cutinase genes during the biotrophic, necrotrophic, and saprotrophic life cycle stages. The gene expression bars represent the average from three biological replicates and error bars are one standard deviation from the mean; dpi, days post-inoculation. Detailed values for all cell wall degrading enzymes are given in supplementary table S2, Supplementary Material online.

Mentions: The transcription analyses are summarized in supplementary table S2, Supplementary Material online. By comparing transcription profiles among members of the same CAZy family, we were able to identify 28 genes displaying life-cycle-specific expression. For example, five of the six genes belonging to the CAZy family carbohydrate esterases 5-encoding cutinases displayed life-cycle-specific expression. ProtID 18212 was preferentially expressed during the biotrophic stage but only marginally expressed during the necrotrophic and saprotrophic stages in the life cycle. ProtID 68483 and ProtID 99331 were expressed mainly in the necrotrophic stage, and ProtID 77282 was expressed mainly during the saprotrophic stage (fig. 1). Similar patterns of life-cycle-specific expression were found in other CAZy families (supplementary fig. S1 and table S2, Supplementary Material online), consistent with the hypothesis of life cycle specialization.Fig. 1.


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)

Standardized transcription values (RPKM) from RNA-Seq experiments in Zymoseptoria tritici indicate differential in planta expression for cutinase genes during the biotrophic, necrotrophic, and saprotrophic life cycle stages. The gene expression bars represent the average from three biological replicates and error bars are one standard deviation from the mean; dpi, days post-inoculation. Detailed values for all cell wall degrading enzymes are given in supplementary table S2, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

mst041-F1: Standardized transcription values (RPKM) from RNA-Seq experiments in Zymoseptoria tritici indicate differential in planta expression for cutinase genes during the biotrophic, necrotrophic, and saprotrophic life cycle stages. The gene expression bars represent the average from three biological replicates and error bars are one standard deviation from the mean; dpi, days post-inoculation. Detailed values for all cell wall degrading enzymes are given in supplementary table S2, Supplementary Material online.
Mentions: The transcription analyses are summarized in supplementary table S2, Supplementary Material online. By comparing transcription profiles among members of the same CAZy family, we were able to identify 28 genes displaying life-cycle-specific expression. For example, five of the six genes belonging to the CAZy family carbohydrate esterases 5-encoding cutinases displayed life-cycle-specific expression. ProtID 18212 was preferentially expressed during the biotrophic stage but only marginally expressed during the necrotrophic and saprotrophic stages in the life cycle. ProtID 68483 and ProtID 99331 were expressed mainly in the necrotrophic stage, and ProtID 77282 was expressed mainly during the saprotrophic stage (fig. 1). Similar patterns of life-cycle-specific expression were found in other CAZy families (supplementary fig. S1 and table S2, Supplementary Material online), consistent with the hypothesis of life cycle specialization.Fig. 1.

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