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Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen.

ABSTRACT: Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this.Here we use single-molecule real-time (SMRT) sequencing to assemble the genome of a prominent fungal wheat pathogen, Fusarium poae, including at least one supernumerary chromosome. The core genome contains limited transposable elements (TEs) and no gene duplications, while the supernumerary genome holds up to 25 % TEs and multiple gene duplications. The core genome shows all hallmarks of repeat-induced point mutation (RIP), a defense mechanism against TEs, specific for fungi. The absence of RIP on the supernumerary genome accounts for the differences between the two (sub)genomes, and results in a functional crosstalk between them. The supernumerary genome is a reservoir for TEs that migrate to the core genome, and even large blocks of supernumerary sequence (>200 kb) have recently translocated to the core. Vice versa, the supernumerary genome acts as a refuge for genes that are duplicated from the core genome.For the first time, a mechanism was determined that explains the differences that exist between the core and supernumerary genome in fungi. Different biology rather than origin was shown to be responsible. A "living apart together" crosstalk exists between the core and supernumerary genome, accelerating chromosomal and organismal evolution.

SUBMITTER: Vanheule A

PROVIDER: S-EPMC4994206 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen.

Vanheule Adriaan A Audenaert Kris K Warris Sven S van de Geest Henri H Schijlen Elio E Höfte Monica M De Saeger Sarah S Haesaert Geert G Waalwijk Cees C van der Lee Theo T

BMC genomics 20160823

<h4>Background</h4>Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this.<h4>Results</h4>Here we use single-molecule rea ...[more]

PMID: 27552804

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Project description:Background: Studying genomic variation in rapidly evolving pathogens potentially enables definition of genes supporting their “core biology” present, functional and expressed by all strains or “flexible biology”, varying between strains. Genes supporting flexible biology may be considered to be “accessory”, whilst the “core” gene set is likely to be important for common features of a pathogen species biology, including virulence on all host genotypes. The wheat-pathogenic fungus Zymoseptoria tritici represents one of the most rapidly evolving threats to global food security and was the focus of this study. Results:We constructed a pangenome of 18 European field isolates, with 12 also subjected to RNAseq transcription profiling during infection. Combining this data, we predicted a “core” gene set comprising 9807 sequences which were; (1) present in all isolates; (2) lacking inactivating polymorphisms ; and (3) expressed by all isolates. A large accessory genome, consisting of 45% of the total genes was also defined. We classified genetic and genomic polymorphism at both chromosomal and individual gene scales. Proteins required for essential functions including virulence, had lower-than average sequence variability amongst core genes. Both core and accessory genomes encoded many small, secreted candidate effector proteins that likely interact with plant immunity. Viral vector-mediated transient in planta overexpression of 88 candidates failed to identify any which induced leaf necrosis characteristic of disease. However, functional complementation of a non-pathogenic deletion mutant lacking five core genes, demonstrated that full virulence was restored by re-introduction of the single gene exhibiting least sequence polymorphism and highest expression. Conclusions:These data support the combined use of pangenomics and transcriptomics for defining genes which represent core, and potentially exploitable, weaknesses in rapidly evolving pathogens.

Dataset Information

Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen.

Publications

Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen.

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