The multi-speed genome of<i>Fusarium oxysporum</i>reveals association of histone modifications with sequence divergence and footprints of past horizontal chromosome transfer events

Fokkens, Like; Shahi, Sabitree; Connolly, Lanelle; Stam, Remco; Schmidt, Sarah M.; Smith, Kristina M.; Freitag, Michael; Rep, Martijn

doi:10.1101/465070

Cited by 46 publications

(84 citation statements)

References 92 publications

(112 reference statements)

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“…This contrasts with the organization of TE-rich regions in Z. tritici, which are enriched with both heterochromatin modifications (43). The situation in Lmb is also different from that of Fusarium oxysporum in which most TE sequences are embedded in H3K27me3-domains (66). We confirmed that, as in most Eukaryotes, H3K4me2-domains are associated with expressed genes while H3K9me3-and H3K27me3-domains are associated with silent genes.…”

Section: Discussionsupporting

confidence: 47%

Genome-Wide Mapping of Histone Modifications in Two Species of Leptosphaeria Maculans Showing Contrasting Genomic Organization and Host Specialization

Soyer¹,

Clairet²,

Lapalu³

et al. 2020

Preprint

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BackgroundIn plant-associated fungi, the epigenome is increasingly recognized as an important regulator of the expression of genes involved in interaction with the host plant. Leptosphaeria maculans ‘brassicae’ (Lmb) and Leptosphaeria maculans ‘lepidii’ (Lml) are closely-related phytopathogenic species that exhibit a large macrosynteny but contrasting genome structure. Lmb has more than 30% of repeats clustered in large repeat-rich regions, while the Lml genome has only a small amount of evenly distributed repeats. Repeat-rich regions of Lmb are enriched in effector genes, expressed during plant infection. The distinct genome structures of Lmb and Lml provide an excellent model for comparing the organization of pathogenicity genes in relation to the chromatin landscape in two closely related phytopathogenic fungi. Here, we performed chromatin immunoprecipitation (ChIP) during axenic culture, targeting histone modifications typical for heterochromatin or euchromatin, combined with transcriptomic analysis to analyse the influence of chromatin organisation on gene expression.ResultsIn both species, we found that facultative heterochromatin are enriched with genes lacking functional annotation, including numerous effector and species-specific genes. Notably, orthologous genes located in H3K27me3-domains are enriched with effector genes. Compared to other fungal species, including Lml, Lmb is distinct in having large H3K9me3-domains associated with repeat-rich regions that contain numerous species-specific effector genes. ConclusionDiscovery of these two distinctive heterochromatin landscapes now raises questions about their involvement in the regulation of pathogenicity, the dynamics of these domains during plant infection, and the selective advantage to the fungus to host effector genes in H3K9me3- or H3K27me3-domains.

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Section: Discussionsupporting

confidence: 47%

Genome-Wide Mapping of Histone Modifications in Two Species of Leptosphaeria Maculans Showing Contrasting Genomic Organization and Host Specialization

Soyer¹,

Clairet²,

Lapalu³

et al. 2020

Preprint

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“…The 5' 9.8-kb subtelomere of contig 22 was at 99. .96% identity to the 5' subtelomeres of contigs 9,15,32,86,87, to a region of contig 107 from positions 9.9 to 19.7 kb, all in forward orientation, and to the 3' subtelomere of contig 30 in reverse orientation.…”

Section: Resultsmentioning

confidence: 98%

“…A DNA helicase regulates mutually exclusive expression of virulence genes in the subtelomeres of Plasmodium falciparum via heterochromatin alteration ). In the asexual pathogen Fusarium oxysporum, SM/pathogenicity gene clusters (facultative heterochromatin) are marked by histone H3 lysine 27 trimethylation (H3K27me3), while euchromatin is marked by histone H3 lysine 4 dimethylation (H3K4me2) (Fokkens et al 2018). Because subtelomeres contain repetitive DNA, their DNA sequences are difficult to reconstruct by genome assembly programs, so they are sparsely represented in databases of whole genome sequence data (Wu et al 2009).…”

Section: Introductionmentioning

confidence: 99%

Host-specific subtelomere: Genomic architecture of pathogen emergence in asexual filamentous fungi

Huang

2019

Preprint

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Several asexual species of filamentous fungal pathogens contain supernumerary chromosomes carrying secondary metabolite (SM) or pathogenicity genes. Supernumerary chromosomes have been shown in in vitro experiments to transfer from pathogenic isolates to non-pathogenic ones and between isolates whose fusion can result in vegetative or heterokaryon incompatibility (HET). However, much is still unknown about the acquisition and maintenance of SM/pathogenicity gene clusters in the adaptation of these asexual pathogens to their hosts. We investigated several asexual fungal pathogens for genomic elements involved in maintaining telomeres for supernumerary and core chromosomes during vegetative reproduction. We found that in vegetative species or lineages with a nearly complete telomere-to-telomere genome assembly (e.g. Fusarium equiseti and five formae speciales of the F. oxysporum species complex), core and supernumerary chromosomes were flanked by highly similar subtelomeric sequences on the 3' side and by their reverse complements on the 5' side. This subtelomere sequence structure was preserved in isolates from the same species or from polyphyletic lineages in the same forma specialis (f.sp.) of the F. oxysporum species complex. Moreover, between some isolates within F. oxysporum f.sp. lycopersici, the mean rate of single nucleotide polymorphisms (SNPs) in a supernumerary chromosome was at least 300 times lower than those in core chromosomes. And a large number of HET domain genes were located in SM/pathogenicity gene clusters, with a potential role in maintaining these gene clusters during vegetative reproduction.

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“…For example, the loss frequency of lineage-specific chromosomes was estimated to be approximately 1 in 35,000 in spores in a liquid culture. Surprisingly, core chromosome 12 in Fol4287 can also be lost but at a very low rate of 1 in 190,000 spores (5,66). In Zymoseptoria tritici , spontaneous accessory chromosome loss rate was much higher with chromosome loss in 2 to >50% of cells during four weeks of incubation (65).…”

Section: Discussionmentioning

confidence: 99%

“…It is well known that repetitive elements can lead to intra- or inter-chromosome homologous recombination, resulting in deletions or translocations (67). It has also been shown that in some fungi the facultative heterochromatin mark H3K27me3 is present in both the subtelomeric regions of the core chromosomes and accessory chromosomes (12,66). This difference in histone modification compared to the core chromosomes may play a role in the difference in chromosome stability (66,68).…”

Section: Discussionmentioning

confidence: 99%

A partial pathogenicity chromosome inFusarium oxysporumis sufficient to cause disease and can be horizontally transferred

Fokkens

Conneely

et al. 2020

Preprint

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During host colonization, plant pathogenic fungi secrete proteins, called effectors, to facilitate infection. Collectively, effectors may defeat the plant immune system, but usually not all effectors are equally important for infecting a particular host plant. In Fusarium oxysporum f.sp. lycopersici, all known effector genes – also called SIX genes – are located on a single accessory chromosome which is required for pathogenicity and can also be horizontally transferred to another strain. To narrow down the minimal region required for virulence, we selected partial pathogenicity chromosome deletion strains by fluorescence-assisted cell sorting of a strain in which the two arms of the pathogenicity chromosome were labelled with GFP and RFP, respectively. By testing the virulence of these deletion mutants, we show that the complete long arm and part of the short arm of the pathogenicity chromosome are not required for virulence. In addition, we demonstrate that smaller versions of the pathogenicity chromosome can also be transferred to a non-pathogenic strain and they are sufficient to turn the non-pathogen into a pathogen. Surprisingly, originally non-pathogenic strains that had received a smaller version of the pathogenicity chromosome were much more aggressive than recipients with a complete pathogenicity chromosome. Whole genome sequencing analysis revealed that partial deletions of the pathogenicity chromosome occurred mainly close to repeats, and that spontaneous duplication of sequences in accessory regions is frequent both in chromosome deletion strains and in horizontal transfer (recipient) strains.Author SummaryFungal genomes can often be divided into a core genome, which is essential for growth, and an accessory genome which is dispensable. The accessory genome in fungi can be beneficial under some conditions. For example, in some plant-pathogenic fungi, virulence genes are present in the accessory genome, which enable these fungi to cause disease on certain hosts. In Fusarium oxysporum f.sp. lycopersici, which infects tomato, all host-specific virulence genes are located on a single accessory chromosome. This ‘pathogenicity chromosome’ can be horizontally transferred between strains. Here, we found that many suspected virulence genes are in fact not required for virulence because strains without a large part of the pathogenicity chromosome, including these genes, showed no reduced virulence. In addition, we demonstrate that partial pathogenicity chromosomes can be horizontally transferred to a non-pathogen. Surprisingly, originally non-pathogenic strains that had received a partial pathogenicity chromosome were more virulent than strains that had received the complete pathogenicity chromosome.

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The multi-speed genome ofFusarium oxysporumreveals association of histone modifications with sequence divergence and footprints of past horizontal chromosome transfer events

Cited by 46 publications

References 92 publications

Genome-Wide Mapping of Histone Modifications in Two Species of Leptosphaeria Maculans Showing Contrasting Genomic Organization and Host Specialization

Genome-Wide Mapping of Histone Modifications in Two Species of Leptosphaeria Maculans Showing Contrasting Genomic Organization and Host Specialization

Host-specific subtelomere: Genomic architecture of pathogen emergence in asexual filamentous fungi

A partial pathogenicity chromosome inFusarium oxysporumis sufficient to cause disease and can be horizontally transferred

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