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

Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan; Yoshikawa-Maekawa, Makoto; Bauer, Saskia; Pedersen, Carsten; Spanu, Pietro D.; Maekawa, Takaki; Schulze-Lefert, Paul; Panstruga, Ralph

doi:10.1186/s12864-018-4750-6

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

Journal Article · 22 May 2018 · BMC Genomics

DOI: https://doi.org/10.1186/s12864-018-4750-6 · OSTI ID:1560553

Frantzeskakis, Lamprinos ^[1]; Kracher, Barbara ^[2]; Kusch, Stefan ^[1]; Yoshikawa-Maekawa, Makoto ^[2]; Bauer, Saskia ^[2]; Pedersen, Carsten ^[3]; Spanu, Pietro D. ^[4]; Maekawa, Takaki ^[2]; Schulze-Lefert, Paul ^[2];

^[1]

RWTH Aachen Univ. (Germany). Inst. for Biology
Max Planck Inst. for Plant Breeding Research, Cologne (Germany)
Univ. of Copenhagen (Denmark). Dept. of Plant and Environmental Sciences
Imperial College, London (United Kingdom). Dept. of Life Sciences

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1560553

Journal Information:: BMC Genomics, Vol. 19, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 87 works

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Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism Saur, Isabel M. L.; Bauer, Saskia; Kracher, Barbara RWTH Aachen University https://doi.org/10.18154/rwth-2019-02172	text	January 2019
The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA Pennington, Helen G.; Jones, Rhian; Kwon, Seomun RWTH Aachen University https://doi.org/10.18154/rwth-2019-02738	text	January 2019
Distinct Life Histories Impact Dikaryotic Genome Evolution in the Rust Fungus Puccinia striiformis Causing Stripe Rust in Wheat Schwessinger, Benjamin; Chen, Yan-Jun; Tien, Richard Genome Biology and Evolution, Vol. 12, Issue 5 https://doi.org/10.1093/gbe/evaa071	journal	April 2020
A chromosome-scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew Müller, Marion C.; Praz, Coraline R.; Sotiropoulos, Alexandros G. Wiley-Blackwell Publishing, Inc. https://doi.org/10.5167/uzh-160633	text	January 2019
Genomic Plasticity Mediated by Transposable Elements in the Plant Pathogenic Fungus Colletotrichum higginsianum Tsushima, Ayako; Gan, Pamela; Kumakura, Naoyoshi Genome Biology and Evolution, Vol. 11, Issue 5 https://doi.org/10.1093/gbe/evz087	journal	April 2019
Novel jack-in-the-box effector of the barley powdery mildew pathogen? Sabelleck, Björn; Panstruga, Ralph Journal of Experimental Botany, Vol. 69, Issue 15 https://doi.org/10.1093/jxb/ery192	journal	June 2018
The haustorial transcriptome of the cucurbit pathogen Podosphaera xanthii reveals new insights into the biotrophy and pathogenesis of powdery mildew fungi Polonio, Álvaro; Seoane, Pedro; Claros, M. Gonzalo BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5938-0	journal	July 2019
Correction to: small RNA discovery in the interaction between barley and the powdery mildew pathogen Hunt, Matt; Banerjee, Sagnik; Surana, Priyanka BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6012-7	journal	September 2019
Network analysis exposes core functions in major lifestyles of fungal and oomycete plant pathogens Pandaranayaka, Eswari PJ; Frenkel, Omer; Elad, Yigal BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6409-3	journal	December 2019
Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States Richards, Jonathan K.; Stukenbrock, Eva H.; Carpenter, Jessica PLOS Genetics, Vol. 15, Issue 10 https://doi.org/10.1371/journal.pgen.1008223	journal	October 2019
The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA Pennington, Helen G.; Jones, Rhian; Kwon, Seomun RWTH Aachen University https://doi.org/10.18154/rwth-2019-02738	text	January 2019
Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle Liang, Peng; Liu, Songyu; Xu, Feng Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03160	journal	December 2018
Collaborative Annotation Redefines Gene Sets for Crucial Phytopathogens Pedro, Helder; Yates, Andrew D.; Kersey, Paul J. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02477	journal	November 2019
Cross-Kingdom RNAi of Pathogen Effectors Leads to Quantitative Adult Plant Resistance in Wheat Schaefer, Luisa Katharina; Parlange, Francis; Buchmann, Gabriele Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00253	journal	March 2020
Transposable Elements Adaptive Role in Genome Plasticity, Pathogenicity and Evolution in Fungal Phytopathogens Mat Razali, Nurhani; Cheah, Boon Huat; Nadarajah, Kalaivani International Journal of Molecular Sciences, Vol. 20, Issue 14 https://doi.org/10.3390/ijms20143597	journal	July 2019
The Many Questions about Mini Chromosomes in Colletotrichum spp. Plaumann, Peter-Louis; Koch, Christian Plants, Vol. 9, Issue 5 https://doi.org/10.3390/plants9050641	journal	May 2020
Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism Saur, Isabel ML; Bauer, Saskia; Kracher, Barbara eLife, Vol. 8 https://doi.org/10.7554/elife.44471	journal	February 2019
Embracing heterogeneity: coalescing the Tree of Life and the future of phylogenomics Bravo, Gustavo A.; Antonelli, Alexandre; Bacon, Christine D. PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6399	journal	January 2019

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Co-evolution
Copy number variation
Effectorome
Evolutionary genomics
Fungal genomics
Host specialization
Synteny
Transposable elements

Additional file 10: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319256 The current record is supplemented by this text	text	January 2018
Additional file 10: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319256.v1 The current record is supplemented by this text	text	January 2018
Additional file 12: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319298 The current record is supplemented by this text	text	January 2018
Additional file 12: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319298.v1 The current record is supplemented by this text	text	January 2018
Additional file 2: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319340 The current record is supplemented by this text	text	January 2018
Additional file 2: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319340.v1 The current record is supplemented by this text	text	January 2018
Additional file 3: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319355 The current record is supplemented by this text	text	January 2018
Additional file 3: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319355.v1 The current record is supplemented by this text	text	January 2018
Additional file 6: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319403.v1 The current record is supplemented by this text	text	January 2018
Additional file7: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319418.v1 The current record is supplemented by this text	text	January 2018
Additional file 8: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319433 The current record is supplemented by this text	text	January 2018
Additional file 8: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319433.v1 The current record is supplemented by this text	text	January 2018
Additional file 9: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319442 The current record is supplemented by this text	text	January 2018
Additional file 9: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319442.v1 The current record is supplemented by this text	text	January 2018
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.c.4108949.v1 The current record is supplemented by this collection	collection	January 2018
Additional file 11: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319274.v1 The current record is supplemented by this text	text	January 2018
Additional file 4: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319370.v1 The current record is supplemented by this text	text	January 2018
Additional file 5: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319388.v1 The current record is supplemented by this text	text	January 2018
Additional file 6: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319403 The current record is supplemented by this text	text	January 2018
Additional file7: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319418 The current record is supplemented by this text	text	January 2018
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.c.4108949 The current record is supplemented by this collection	collection	January 2018
Additional file 11: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319274 The current record is supplemented by this text	text	January 2018
Additional file 1: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319319 The current record is supplemented by this dataset	dataset	January 2018
Additional file 4: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319370 The current record is supplemented by this text	text	January 2018
Additional file 1: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319319.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 5: of Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan https://doi.org/10.6084/m9.figshare.6319388 The current record is supplemented by this text	text	January 2018