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

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

Patrick C Brunner et al. Mol Biol Evol. 2013 Jun.

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.

Keywords: adaptive evolution; coevolution; host adaptation; natural selection.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.

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.

F<sc>ig</sc>. 2.
Fig. 2.

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.

F<sc>ig</sc>. 3.
Fig. 3.

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 null-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.

F<sc>ig</sc>. 4.
Fig. 4.

Categorization of PCWDEs according to the four main evolutionary scenarios postulated to affect their evolution (see also fig. 5). Only significant differences in transcript abundances among the different life stages are highlighted. The fifth column identifies the 13 enzymes that could not be categorized.

F<sc>ig</sc>. 5.
Fig. 5.

Schematic visualization of the four main evolutionary scenarios postulated to affect the evolution of PCWDEs in plant pathogenic fungi (yellow circles). Different hosts are represented by different leaf shapes. Different symbols indicate PCWDEs belonging to the same gene family and colors represent different alleles (protein variants) of a specific gene. 1) Life cycle specialization: Members of the same gene family are preferentially expressed at different stages of the pathogen life cycle. 2) Host adaptation: Purifying selection for different protein variants of the same gene on different hosts. 3) Host evasion: Recognition of a specific protein (blue) by the host and subsequent diversifying selection on the same protein to evade recognition. 4) Conserved substrate optimization: Purifying selection for the same optimized protein variant on different hosts.

F<sc>ig</sc>. 6.
Fig. 6.

Standardized transcription values (RPKM) for cell wall degrading enzymes in Zymoseptoria tritici that showed significant values of diversifying or purifying selection according to McDonald–Kreitman tests. Genes are color-coded according to the evolutionary scenario to which they were assigned (see also figs. 4 and 5). 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 are given in

supplementary table S2

,

Supplementary Material

online.

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