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Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle.

ABSTRACT: Powdery mildew is a widespread plant disease caused by obligate biotrophic fungal pathogens involving species-specific interactions between host and parasite. To gain genomic insights into the underlying obligate biotrophic mechanisms, we analyzed 15 microbial genomes covering powdery and downy mildews and rusts. We observed a genome-wide, massive contraction of multiple gene families in powdery mildews, such as enzymes in the carbohydrate metabolism pathway, when compared with ascomycete phytopathogens, while the fatty acid metabolism pathway maintained its integrity. We also observed significant differences in candidate secreted effector protein (CSEP) families between monocot and dicot powdery mildews, perhaps due to different selection forces. While CSEPs in monocot mildews are likely subject to positive selection causing rapid expansion, CSEP families in dicot mildews are shrinking under strong purifying selection. Our results not only illustrate obligate biotrophic mechanisms of powdery mildews driven by gene family evolution in nutrient metabolism, but also demonstrate how the divergence of CSEPs between monocot and dicot lineages might contribute to species-specific adaption.

SUBMITTER: Liang P

PROVIDER: S-EPMC6305591 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle.

Liang Peng P Liu Songyu S Xu Feng F Jiang Shuqin S Yan Jun J He Qiguang Q Liu Wenbo W Lin Chunhua C Zheng Fucong F Wang Xiangfeng X Miao Weiguo W

Frontiers in microbiology 20181218

Powdery mildew is a widespread plant disease caused by obligate biotrophic fungal pathogens involving species-specific interactions between host and parasite. To gain genomic insights into the underlying obligate biotrophic mechanisms, we analyzed 15 microbial genomes covering powdery and downy mildews and rusts. We observed a genome-wide, massive contraction of multiple gene families in powdery mildews, such as enzymes in the carbohydrate metabolism pathway, when compared with <i>ascomycete</i> ...[more]

PMID: 30619222

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Project description:BackgroundGrass powdery mildew (Blumeria graminis, Ascomycota) is a major pathogen of cereal crops and has become a model organism for obligate biotrophic fungal pathogens of plants. The sequenced genomes of two formae speciales (ff.spp.), B.g. hordei and B.g. tritici (pathogens of barley and wheat), were found to be enriched in candidate effector genes (CEGs). Similar to other filamentous pathogens, CEGs in B. graminis are under positive selection. Additionally, effectors are more likely to have presence-absence polymorphisms than other genes among different strains.ResultsHere we identified effectors in the genomes of three additional host-specific lineages of B. graminis (B.g. poae, B.g. avenae and B.g. infecting Lolium) which diverged between 24 and 5 million years ago (Mya). We found that most CEGs in B. graminis are clustered in families and that most families are present in both reference genomes (B.g. hordei and B.g. tritici) and in the genomes of all three newly annotated lineages. We identified conserved protein domains including a novel lipid binding domain. The phylogenetic analysis showed that frequent gene duplications and losses shaped the diversity of the effector repertoires of the different lineages through their evolutionary history. We observed several lineage-specific expansions where large clades of CEGs originated in only one lineage from a single gene through repeated gene duplications. When we applied a birth-death model we found that the turnover rate (the rate at which genes are deleted and duplicated) of CEG families is much higher than for non-CEG families. The analysis of genomic context revealed that the immediate surroundings of CEGs are enriched in transposable elements (TE) which could play a role in the duplication and deletion of CEGs.ConclusionsThe CEG repertoires of related pathogens diverged dramatically in short evolutionary times because of rapid turnover and of positive selection fixing non-synonymous mutations. While signatures of positive selection on effector sequences are the expected outcome of the evolutionary "arms race" between pathogen and plant immune system, it is more difficult to infer the mechanisms and evolutionary forces that maintained an extreme turnover rate in CEG families of B. graminis for several millions of years.

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Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle.

Publications

Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle.

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