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Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data.

ABSTRACT: Blumeria graminis (Ascomycota) includes fungal pathogens that infect numerous grasses and cereals. Despite its economic impact on agriculture and its scientific importance in plant-pathogen interaction studies, the evolution of different lineages with different host ranges is poorly understood. Moreover, the taxonomy of grass powdery mildew is rather exceptional: there is only one described species (B. graminis) subdivided in different formae speciales (ff.spp.), which are defined by their host range. In this study we applied phylogenomic and population genomic methods to whole genome sequence data of 31 isolates of B. graminis belonging to different ff.spp. and reconstructed the evolutionary relationships between different lineages. The results of the phylogenomic analysis support a pattern of co-evolution between some of the ff.spp. and their host plant. In addition, we identified exceptions to this pattern, namely host jump events and the recent radiation of a clade less than 280,000 years ago. Furthermore, we found a high level of gene tree incongruence localized in the youngest clade. To distinguish between incomplete lineage sorting and lateral gene flow, we applied a coalescent-based method of demographic inference and found evidence of horizontal gene flow between recently diverged lineages. Overall we found that different processes shaped the diversification of B. graminis, co-evolution with the host species, host jump and fast radiation. Our study is an example of how genomic data can resolve complex evolutionary histories of cryptic lineages at different time scales, dealing with incomplete lineage sorting and lateral gene flow.

SUBMITTER: Menardo F

PROVIDER: S-EPMC5381671 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data.

Menardo Fabrizio F Wicker Thomas T Keller Beat B

Genome biology and evolution 20170201 2

Blumeria graminis (Ascomycota) includes fungal pathogens that infect numerous grasses and cereals. Despite its economic impact on agriculture and its scientific importance in plant-pathogen interaction studies, the evolution of different lineages with different host ranges is poorly understood. Moreover, the taxonomy of grass powdery mildew is rather exceptional: there is only one described species (B. graminis) subdivided in different formae speciales (ff.spp.), which are defined by their host ...[more]

PMID: 28164219

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Project description:Grass 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.Here 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.The 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.

Project description:Powdery mildews are biotrophic pathogens causing fungal diseases in many economically important crops, including cereals, which are affected by Blumeria graminis. Powdery mildews only invade the epidermal cell layer of leaf tissues, in which they form haustorial structures. Haustoria are at the center of the biotrophic interaction by taking up nutrients from the host and by delivering effectors in the invaded cells to jeopardize plant immunity. Haustoria are composed of a fungal core delimited by a haustorial plasma membrane and cell wall. Surrounding these is the extrahaustorial complex, of which the extrahaustorial membrane is of plant origin. Although haustoria transcriptomes and proteomes have been investigated for Blumeria, the proteomes of barley epidermis upon infection and the barley components of the extrahaustorial complex remains unexplored. When comparing proteomes of infected and non-infected epidermis, several classical pathogenesis-related (PR) proteins were more abundant in infected epidermis. These included peroxidases, chitinases, cysteine-rich venom secreted proteins/PR1 and two thaumatin-like PR5 protein isoforms, of which TLP5 was previously shown to interact with the Blumeria effector BEC1054 (CSEP0064). Against expectations, transient TLP5 gene silencing suggested that TLP5 does not contribute to resistance but modulates susceptibility towards B. graminis. In a second proteomics comparison, haustorial structures were enriched from infected epidermal strips to identify plant proteins closely associated with the extrahaustorial complex. In these haustoria-enriched samples, relative abundances were higher for several V-type ATP synthase/ATPase subunits, suggesting the generation of proton gradients in the extrahaustorial space. Other haustoria-associated proteins included secreted or membrane proteins such as a PIP2 aquaporin, an early nodulin-like protein 9, an aspartate protease and other proteases, a lipase, and a lipid transfer protein, all of which are potential modulators of immunity, or the targets of pathogen effectors. Moreover, the ER BIP-like HSP70, may link ER stress responses and the idea of ER-like properties previously attributed to the extrahaustorial membrane. This initial investigation exploring the barley proteomes of Blumeria-infected tissues and haustoria, associated with a transient gene silencing approach, is invaluable to gain first insight of key players of resistance and susceptibility.

Dataset Information

Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data.

Publications

Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data.

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