Repeat-Induced Point Mutation and Other Genome Defense Mechanisms in Fungi

Gladyshev, Eugene

doi:10.1128/microbiolspec.funk-0042-2017

Cited by 121 publications

(112 citation statements)

References 92 publications

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“…However, the highly negative correlation did not hold in the mini-chromosome, which is highly repetitive while maintaining relatively high GC content. Repetitive sequences in many fungi are subject to repeat-induced point (RIP) mutation resulting in C-to-T or G-to-A transitions and, thereby, leading to reduced GC content (NAKAYASHIKI et al 1999;IKEDA et al 2002;HANE AND OLIVER 2008;GLADYSHEV 2017). Given higher GC content of repetitive sequences in the minichromosome versus core chromosomes, we explored the possibility of different levels of RIP in these genomic regions, as observed in Fusarium mini-chromosomes (VANHEULE et al 2016), by assessing their RIP-type mutation rates.…”

Section: Repetitive Sequences In B71 Core-and Mini-chromosomesmentioning

confidence: 99%

Effector Gene Reshuffling Involves Dispensable Mini-chromosomes in the Wheat Blast Fungus

Peng

Oliveira-Garcia

Lin

et al. 2018

Preprint

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Newly emerged wheat blast disease is a serious threat to global wheat production. Wheat blast is caused by a distinct, exceptionally diverse lineage of the fungus causing rice blast disease. To understand genetic diversity in wheat-infecting strains, we report a near-finished reference genome of a recent field isolate generated using long read sequencing and a novel scaffolding approach with long-distance paired genomic sequences. The genome assemblage includes seven core chromosomes and sequences from a dispensable mini-chromosome that harbors effector genes normally found on the ends of core chromosomes in other strains. No mini-chromosomes were observed in an early field strain, and two mini-chromosomes from another field isolate each contain different effector homologous genes and core chromosome end sequences. The minichromosome is highly repetitive and is enriched in transposons occurring most frequently at core chromosome ends. Additionally, transposons in mini-chromosomes lack the characteristic signature for inactivation by repeat-induced point (RIP) mutation genome defenses. Our results, collectively, indicate that dispensable mini-chromosomes and non-dispensable core chromosomes undergo divergent evolutionary trajectories, and mini-chromosomes and core chromosome ends are coupled as a mobile, fast-evolving effector compartment in the wheat pathogen genome. Significance statementThe emerging blast disease on wheat is proving even harder to control than the ancient, stillproblematic rice blast disease. Potential wheat resistance identified using strains isolated soon after disease emergence are no longer effective in controlling recent aggressive field isolates from wheat in South America and South Asia. We report that recent wheat pathogens can contain 3 one or two highly-variable conditionally-dispensable mini-chromosomes, each with an amalgamation of effector sequences that are duplicated or absent from pathogen core chromosome ends. Well-studied effectors found on different core chromosomes in rice pathogens appear side-by-side in wheat pathogen mini-chromosomes. The rice pathogen often overcomes deployed resistance genes by deleting triggering effector genes. Localization of effectors on mini-chromosomes, which are unstably transmitted during growth, would accelerate pathogen adaptation in the field. aggressive wheat pathogens that are so far restricted to certain countries in South America and South Asia (Fig. 1A).Although little is known about wheat blast, studies on rice blast disease have identified numerous effector genes, generally encoding small proteins that are specifically expressed in planta and play roles in host invasion (GIRALDO AND VALENT 2013). Some effectors, termed avirulence (AVR) effectors, determine either rice cultivar or host species specificity through blocking infection upon recognition by corresponding cultivar-or species-specific resistance (R) genes and triggering hypersensitive resistance. For example, strains of several M. oryzae pathotypes are able to infect weeping lo...

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Section: Repetitive Sequences In B71 Core-and Mini-chromosomesmentioning

confidence: 99%

Effector Gene Reshuffling Involves Dispensable Mini-chromosomes in the Wheat Blast Fungus

Peng

Oliveira-Garcia

Lin

et al. 2018

Preprint

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“…We hypothesised that repeat induced point mutation (RIP), a natural genome defence mechanism operating in many sexual fungi, could be harnessed for this purpose. RIP causes C→T muta ons in sequences that contain repeats greater than ~400 bp (Gladyshev, 2017) located anywhere in the genome. The recognition and mutation of repetitive sequences within the parental nucleus occurs following cell fusion but prior to nuclear fusion during meiosis (Gladyshev, 2017).…”

Section: Selfing Is Not Necessarily An Impediment To Drive Spreadmentioning

confidence: 99%

“…RIP causes C→T muta ons in sequences that contain repeats greater than ~400 bp (Gladyshev, 2017) located anywhere in the genome. The recognition and mutation of repetitive sequences within the parental nucleus occurs following cell fusion but prior to nuclear fusion during meiosis (Gladyshev, 2017). RIP is moderately active in F. graminearum (Pomraning et al, 2013) and likely to have been a key process in shaping the repeat-poor genome of this species (Cuomo et al, 2007).…”

Section: Selfing Is Not Necessarily An Impediment To Drive Spreadmentioning

confidence: 99%

Natural gene drives offer potential pathogen control strategies in plants

Gardiner

Rusu

Barrett

et al. 2020

Preprint

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SummaryGlobally, fungal pathogens cause enormous crop losses and current control practices are not always effective, economical or environmentally sustainable. Tools enabling genetic management of wild pathogen populations could potentially solve many problems associated with plant diseases.A natural gene drive from a heterologous species can be used in the globally important cereal pathogen, Fusarium graminearum, to remove pathogenic traits from contained populations of the fungus. The gene drive element became fixed in a freely crossing populations in only three generations.Repeat induce point mutation, a natural genome defence mechanism in fungi, may be useful to recall the gene drive following release, should a failsafe mechanism be required.We propose that gene drive technology is a potential tool to control plant pathogens.

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“…The patchwork structure of this genome may partially obviate the need for sequence motifs to recruit proteins that define TAD boundaries. There is evidence that the molecular machinery associated with RIP can detect repetitive elements and mark them with methylated cytosines, which, in turn, could drive the formation and spread of condensed chromatin around these repeat regions (Gladyshev 2017;Gladyshev & Kleckner 2017). Under this model, the condensed chromatin states formed by the AT-rich blocks would act to insulate the relatively open chromatin loops of the gene-rich blocks from each other, thus naturally creating TAD-like structures in the genome (Figure 9).…”

Section: A Finished Reference Genome For Genus Epichloëmentioning

confidence: 99%

Repeat elements organize 3D genome structure and mediate transcription in the filamentous fungusEpichloë festucae

Winter

Ganley

Young

et al. 2018

Preprint

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Structural features of genomes, including the three-dimensional arrangement of DNA in the nucleus, are increasingly seen as key contributors to the regulation of gene expression. However, studies on how genome structure and nuclear organization influence transcription have so far been limited to a handful of model species. This narrow focus limits our ability to draw general conclusions about the ways in which three-dimensional structures are encoded, and to integrate information from three-dimensional data to address a broader gamut of biological questions. Here, we generate a complete and gapless genome sequence for the filamentous fungus, Epichloë festucae. Coupling it with RNAseq and HiC data, we investigate how the structure of the genome contributes to the suite of transcriptional changes that an Epichloë species needs to maintain symbiotic relationships with its grass host. Our results reveal a unique "patchwork" genome, in which repeat-rich blocks of DNA with discrete boundaries are interspersed by gene-rich sequences. In contrast to other species, the three-dimensional structure of the genome is anchored by these repeat blocks, which act to isolate transcription in neighbouring gene-rich regions. Genes that are differentially expressed in planta are enriched near the boundaries of these repeat-rich blocks, suggesting that their three-dimensional orientation partly encodes and regulates the symbiotic relationship formed by this organism.A total of 6,709 base-level errors, mostly single base indels (96.9%), were polished using the Pilon finisher with 87x coverage Illumina paired-end sequencing as input. Finally, telomeres were trimmed to the nearest canonical sequence and, where necessary, chromosome sequences were reverse-complemented to place the short arm of the chromosome first by

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Repeat-Induced Point Mutation and Other Genome Defense Mechanisms in Fungi

Cited by 121 publications

References 92 publications

Effector Gene Reshuffling Involves Dispensable Mini-chromosomes in the Wheat Blast Fungus

Effector Gene Reshuffling Involves Dispensable Mini-chromosomes in the Wheat Blast Fungus

Natural gene drives offer potential pathogen control strategies in plants

Repeat elements organize 3D genome structure and mediate transcription in the filamentous fungusEpichloë festucae

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