Repeat-induced point mutation in Neurospora crassa causes the highest known mutation rate and mutational burden of any cellular life

Wang, Long; Sun, Yingying; Sun, Xiaoguang; Yu, Luyao; Xue, L.; He, Zhen; Huang, Ju; Tian, Dacheng; Hurst, Laurence D.; Yang, Sihai

doi:10.1186/s13059-020-02060-w

Cited by 34 publications

(82 citation statements)

References 45 publications

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“…RIP mutations have been associated with meiosis, but alternative mechanisms during vegetative propagation could lead to RIP-like mutations (Clutterbuck 2011). This has been recently observed in Z. tritici and N. crassa in which propagation through mitotic divisions generate RIP-like mutations Wang, et al 2020). Intriguingly, dynamic TEs are depleted in RIP mutations.…”

Section: Discussionmentioning

confidence: 54%

“…Furthermore, TE activities are generally suppressed by host defense processes. These processes include DNA methylation (Selker, et al 2003;Zemach, et al 2010), histone modifications associated with highly condensed heterochromatin (Slotkin and Martienssen 2007;Hocher, et al 2018;Hocher and Taddei 2020), targeted processes such as RNA-silencing (Lippman and Martienssen 2004;Nicolas, et al 2013;Yadav, et al 2018), or repeat-induced point (RIP) mutation (Cambareri, et al 1989; Galagan and Selker 2004;Fudal, et al 2009;Wang, et al 2020).…”

Section: Introductionmentioning

confidence: 99%

“…Changes in mutation rates in genes in proximity TEs can be caused by leakage of TE silencing mechanisms (e.g. RIP) or DNA repair following TE insertion (Fudal, et al 2009;Rouxel, et al 2011;Yoshida, et al 2016;Wang, et al 2020). Furthermore, abundant TEs and other repetitive elements can act as an ectopic substrate for double-strand break repair pathways, thereby fostering chromosomal rearrangements (structural variants; SVs), such as chromosomal translocations and inversions as well as large-scale duplications and deletions (Chan and Kolodner 2011;Faino, et al 2016;Bourque, et al 2018).…”

Section: Introductionmentioning

confidence: 99%

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Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Torres

Thomma

Seidl

2021

Preprint

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Transposable elements (TEs) are a major source of genetic and regulatory variation in their host genome and are consequently thought to play important roles in evolution. Many fungal and oomycete plant pathogens have evolved dynamic and TE-rich genomic regions containing genes that are implicated in host colonization. TEs embedded in these regions have typically been thought to accelerate the evolution of these genomic compartments, but little is known about their dynamics in strains that harbor them. Here, we used whole-genome sequencing data of 42 strains of the fungal plant pathogen Verticillium dahliae to systematically identify polymorphic TEs that may be implicated in genomic as well as in gene expression variation. We identified 2,523 TE polymorphisms and characterize a subset of 8% of the TEs as dynamic elements that are evolutionary younger, less methylated, and more highly expressed when compared with the remaining 92% of the TE complement. As expected, the dynamic TEs are enriched in the dynamic genomic regions. Besides, we observed an association of dynamic TEs with pathogenicity-related genes that localize nearby and that display high expression levels. Collectively, our analyses demonstrate that TE dynamics in V. dahliae contributes to genomic variation, correlates with expression of pathogenicity-related genes, and potentially impacts the evolution of dynamic genomic regions.Significance statementTransposable elements (TEs) are ubiquitous components of genomes and are major sources of genetic and regulatory variation. Many plant pathogens have evolved TE-rich genomic regions containing genes with roles in host colonization, and TEs are thought to contribute to accelerated evolution of these dynamic regions. We analyzed the fungal plant pathogen Verticillium dahliae to identify TE variation between strains and to demonstrate that polymorphic TEs have specific characteristic that separates them from the majority of TEs. Polymorphic TEs are enriched in dynamic genomic regions and are associated with structural variants and highly expressed pathogenicity-related genes. Collectively, our results provide evidence for the hypothesis that dynamic TEs contribute to increased genomic diversity, functional variation, and the evolution of dynamic genomic regions.

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Section: Discussionmentioning

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Torres

Thomma

Seidl

2021

Preprint

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“…The longest of those stretches poor in both heterozygous and homozygous positions was found on chromosome 4, and corresponded to a region rich in both genes and repeat elements. This is remarkable and probably due to a recent proliferation, as repeat-rich regions are usually less stable and more prone to accumulate mutations [78][79][80].…”

Section: Distribution Of Single Nucleotide Polymorphisms (Snps)mentioning

confidence: 99%

A chromosome-level genome assembly of the European Beech (Fagus sylvatica) reveals anomalies for organelle DNA integration, repeat content and distribution of SNPs

Mishra

Ulaszewski

Meger

et al. 2021

Preprint

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Background: The European Beech is the dominant climax tree in most regions of Central Europe and valued for its ecological versatility and hardwood timber. Even though a draft genome has been published recently, higher resolution is required for studying aspects of genome architecture and recombination. Results: Here we present a chromosome-level assembly of the more than 300 year-old reference individual, Bhaga, from the Kellerwald-Edersee National Park (Germany). Its nuclear genome of 541 Mb was resolved into 12 chromosomes varying in length between 28 Mb and 73 Mb. Multiple nuclear insertions of parts of the chloroplast genome were observed, with one region on chromosome 11 spanning more than 2 Mb of the genome in which fragments up to 54,784 bp long and covering the whole chloroplast genome were inserted randomly. Unlike in Arabidopsis thaliana, ribosomal cistrons are present in Fagus sylvatica only in four major regions, in line with FISH studies. On most assembled chromosomes, telomeric repeats were found at both ends, while centromeric repeats were found to be scattered throughout the genome apart from their main occurrence per chromosome. The genome-wide distribution of SNPs was evaluated using a second individual from Jamy Nature Reserve (Poland). SNPs, repeat elements and duplicated genes were unevenly distributed in the genomes, with one major anomaly on chromosome 4. Conclusions: The genome presented here adds to the available highly resolved plant genomes and we hope it will serve as a valuable basis for future research on genome architecture and for understanding the past and future of European Beech populations in a changing climate.

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“…The transposition of TEs can disrupt coding sequences or change the regulation of effector genes (Sánchez-Vallet et al, 2018;Meile et al, 2018;Fouché et al, 2020). Additionally, repetitive sequences can lead to higher mutation rates through a mechanism known as repeat induced point (RIP) mutation (Gladyshev, 2017;Gardiner et al, 2020;Wang et al, 2020). Brassica napus (canola) carrying the Rlm1 resistance gene suffered a breakdown of resistance against the fungal pathogen Leptosphaeria maculans (Van de Wouw et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen

Singh

Badet

Croll

2021

Preprint

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Background: Plant pathogens cause substantial crop losses in agriculture production and threaten food security. Plants evolved the ability to recognize virulence factors and pathogens have repeatedly escaped recognition due rapid evolutionary change at pathogen virulence loci (i.e. effector genes). The presence of transposable elements (TEs) in close physical proximity of effector genes can have important consequences for gene regulation and sequence evolution. Species-wide investigations of effector gene loci remain rare hindering our ability to predict pathogen evolvability.Results: Here, we performed genome-wide association studies (GWAS) on a highly polymorphic mapping population of 120 isolates of Zymoseptoria tritici, the most damaging pathogen of wheat in Europe. We identified a major locus underlying significant variation in reproductive success of the pathogen and damage caused on the wheat cultivar Claro. The most strongly associated locus is intergenic and flanked by genes encoding a predicted effector and a serine type protease, respectively. The center of the locus contained a highly dynamic region consisting of multiple families of TEs. Based on a large global collection of assembled genomes, we show that the virulence locus has undergone substantial recent sequence evolution. Large insertion and deletion events generated length variation between the flanking genes by a factor of seven (5–35 kb). The locus showed also strong signatures of genomic defenses against TEs (i.e. RIP) contributing to the rapid diversification of the locus.Conclusions: In conjunction, our work highlights the power of combining GWAS and population-scale genome analyses to investigate major effect loci in pathogens.

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Repeat-induced point mutation in Neurospora crassa causes the highest known mutation rate and mutational burden of any cellular life

Cited by 34 publications

References 45 publications

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

A chromosome-level genome assembly of the European Beech (Fagus sylvatica) reveals anomalies for organelle DNA integration, repeat content and distribution of SNPs

Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen

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