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Title: Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen

Abstract

BACKGROUND: Powdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants. The grass powdery mildew, Blumeria graminis, has become a model organism to study host specialization of obligate biotrophic fungal pathogens. We resolved the large-scale genomic architecture of B. graminis forma specialis hordei (Bgh) to explore the potential influence of its genome organization on the co-evolutionary process with its host plant, barley (Hordeum vulgare). RESULTS: The near-chromosome level assemblies of the Bgh reference isolate DH14 and one of the most diversified isolates, RACE1, enabled a comparative analysis of these haploid genomes, which are highly enriched with transposable elements (TEs). We found largely retained genome synteny and gene repertoires, yet detected copy number variation (CNV) of secretion signal peptide-containing protein-coding genes (SPs) and locally disrupted synteny blocks. Genes coding for sequence-related SPs are often locally clustered, but neither the SPs nor the TEs reside preferentially in genomic regions with unique features. Extended comparative analysis with different host-specific B. graminis formae speciales revealed the existence of a core suite of SPs, but also isolate-specific SP sets as well as congruence of SP CNV and phylogenetic relationship. We further detected evidence for a recent, lineage-specific expansion of TEs in themore » Bgh genome. CONCLUSIONS: The characteristics of the Bgh genome (largely retained synteny, CNV of SP genes, recently proliferated TEs and a lack of significant compartmentalization) are consistent with a "one-speed" genome that differs in its architecture and (co-)evolutionary pattern from the "two-speed" genomes reported for several other filamentous phytopathogens.« less

Authors:
 [1];  [2];  [1];  [2];  [2];  [3];  [4];  [2];  [2]; ORCiD logo [1]
  1. RWTH Aachen Univ. (Germany). Inst. for Biology
  2. Max Planck Inst. for Plant Breeding Research, Cologne (Germany)
  3. Univ. of Copenhagen (Denmark). Dept. of Plant and Environmental Sciences
  4. Imperial College, London (United Kingdom). Dept. of Life Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1560553
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Co-evolution; Copy number variation; Effectorome; Evolutionary genomics; Fungal genomics; Host specialization; Synteny; Transposable elements

Citation Formats

Frantzeskakis, Lamprinos, Kracher, Barbara, Kusch, Stefan, Yoshikawa-Maekawa, Makoto, Bauer, Saskia, Pedersen, Carsten, Spanu, Pietro D., Maekawa, Takaki, Schulze-Lefert, Paul, and Panstruga, Ralph. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. United States: N. p., 2018. Web. doi:10.1186/s12864-018-4750-6.
Frantzeskakis, Lamprinos, Kracher, Barbara, Kusch, Stefan, Yoshikawa-Maekawa, Makoto, Bauer, Saskia, Pedersen, Carsten, Spanu, Pietro D., Maekawa, Takaki, Schulze-Lefert, Paul, & Panstruga, Ralph. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. United States. https://doi.org/10.1186/s12864-018-4750-6
Frantzeskakis, Lamprinos, Kracher, Barbara, Kusch, Stefan, Yoshikawa-Maekawa, Makoto, Bauer, Saskia, Pedersen, Carsten, Spanu, Pietro D., Maekawa, Takaki, Schulze-Lefert, Paul, and Panstruga, Ralph. Tue . "Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen". United States. https://doi.org/10.1186/s12864-018-4750-6. https://www.osti.gov/servlets/purl/1560553.
@article{osti_1560553,
title = {Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen},
author = {Frantzeskakis, Lamprinos and Kracher, Barbara and Kusch, Stefan and Yoshikawa-Maekawa, Makoto and Bauer, Saskia and Pedersen, Carsten and Spanu, Pietro D. and Maekawa, Takaki and Schulze-Lefert, Paul and Panstruga, Ralph},
abstractNote = {BACKGROUND: Powdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants. The grass powdery mildew, Blumeria graminis, has become a model organism to study host specialization of obligate biotrophic fungal pathogens. We resolved the large-scale genomic architecture of B. graminis forma specialis hordei (Bgh) to explore the potential influence of its genome organization on the co-evolutionary process with its host plant, barley (Hordeum vulgare). RESULTS: The near-chromosome level assemblies of the Bgh reference isolate DH14 and one of the most diversified isolates, RACE1, enabled a comparative analysis of these haploid genomes, which are highly enriched with transposable elements (TEs). We found largely retained genome synteny and gene repertoires, yet detected copy number variation (CNV) of secretion signal peptide-containing protein-coding genes (SPs) and locally disrupted synteny blocks. Genes coding for sequence-related SPs are often locally clustered, but neither the SPs nor the TEs reside preferentially in genomic regions with unique features. Extended comparative analysis with different host-specific B. graminis formae speciales revealed the existence of a core suite of SPs, but also isolate-specific SP sets as well as congruence of SP CNV and phylogenetic relationship. We further detected evidence for a recent, lineage-specific expansion of TEs in the Bgh genome. CONCLUSIONS: The characteristics of the Bgh genome (largely retained synteny, CNV of SP genes, recently proliferated TEs and a lack of significant compartmentalization) are consistent with a "one-speed" genome that differs in its architecture and (co-)evolutionary pattern from the "two-speed" genomes reported for several other filamentous phytopathogens.},
doi = {10.1186/s12864-018-4750-6},
journal = {BMC Genomics},
number = 1,
volume = 19,
place = {United States},
year = {Tue May 22 00:00:00 EDT 2018},
month = {Tue May 22 00:00:00 EDT 2018}
}

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Figures / Tables:

Table 1 Table 1: Assembly statistics for the genomes of the Bgh isolates DH14 and RACE1

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Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States
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Collaborative Annotation Redefines Gene Sets for Crucial Phytopathogens
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Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.