A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species

Dam, Peter van; Fokkens, Like; Ayukawa, Yu; Gragt, Michelle van der; Horst, Anneliek ter; Brankovics, Balázs; Houterman, Petra M.; Arie, Tsutomu; Rep, Martijn

doi:10.1038/s41598-017-07995-y

Cited by 134 publications

(182 citation statements)

References 62 publications

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“…Based on these findings, the 'two-speed genome' hypothesis was proposed, which states that the compartments rich in effector genes evolve at a faster pace than the rest of the genome (Dong et al, 2015;Wang et al, 2017). For example, in Fusarium oxysporum, effectors are preferably located on repeatrich accessory chromosomes (van Dam et al, 2017), whereas in Leptosphaeria maculans and Phytophthora infestans the effectors are found in repeat-rich regions of the core chromosomes (Dong et al, 2015). It is assumed that mutation rates in effectors can be locally increased if they are near transposable elements (TEs) that are silenced through the repeat-induced point mutation (RIP) pathway (Fudal et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

et al. 2018

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Summary Blumeria graminis f. sp. tritici ( B.g. tritici ) is the causal agent of the wheat powdery mildew disease. The highly fragmented B.g. tritici genome available so far has prevented a systematic analysis of effector genes that are known to be involved in host adaptation. To study the diversity and evolution of effector genes we produced a chromosome‐scale assembly of the B.g. tritici genome. The genome assembly and annotation was achieved by combining long‐read sequencing with high‐density genetic mapping, bacterial artificial chromosome fingerprinting and transcriptomics. We found that the 166.6 Mb B.g. tritici genome encodes 844 candidate effector genes, over 40% more than previously reported. Candidate effector genes have characteristic local genomic organization such as gene clustering and enrichment for recombination‐active regions and certain transposable element families. A large group of 412 candidate effector genes shows high plasticity in terms of copy number variation in a global set of 36 isolates and of transcription levels. Our data suggest that copy number variation and transcriptional flexibility are the main drivers for adaptation in B.g. tritici . The high repeat content may play a role in providing a genomic environment that allows rapid evolution of effector genes with selection as the driving force.

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Section: Introductionmentioning

confidence: 99%

A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

et al. 2018

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“…In F. oxysporum f.sp. radicis-cucumerinum (Forc) isolate Forc016, its genome assembly consisted of 11 core chromosomes, one supernumerary chromosome (chromosome RC), and a number of unplaced contigs (van Dam et al 2017). Chromosome RC, assembled from telomere to telomere, was flanked on either side by 13-kb complementary sequences at 99.96% complementarity ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Another connection between core subtelomeres and supernumerary chromosomes is that they are enriched with a silencing histone modification, trimethylation of lysine 27 on histone H3 protein subunit (H3K27me3) (Galazka and Freitag 2014). Supernumerary chromosomes have been shown in in vitro experiments to transfer between vegetatively incompatible isolates or to transfer from a pathogenic isolate to a non-pathogenic isolate (Horizontal Chromosome Transfer or HCT) in asexual filamentous fungi (He et al 1998;Akagi et al 2009;Ma et al 2010;Vlaardingerbroek et al 2016a;van Dam et al 2017). A phylogenetic analysis of core genes and supernumerary effector genes suggests horizontal transfer of these effector genes (van Dam et al 2016).…”

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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“…Ma et al (2010) demonstrated that the LS regions observed in the whole genome of Fol had a phylogenetic origin independent of the core genome, and the LS regions could be horizontally transferred. Multiple studies have since hypothesized that the SIX genes, located on the LS regions, have been horizontally transferred between formae speciales of F. oxysporum, and that horizontal gene transfer (HGT) explains the dual poly-and monophylogeny observed in many formae speciales (Fraser-Smith et al, 2014;Laurence et al, 2015;Taylor et al, 2016;van Dam et al, 2017;Czislowski et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Ma et al (2010) then demonstrated the LS regions of Fol could be horizontally transferred to a nonpathogenic strain, transforming it into a pathogen. Multiple studies have since hypothesized that the SIX genes have been horizontally transferred between formae speciales of F. oxysporum (Fraser-Smith et al, 2014;Laurence et al, 2015;Taylor et al, 2016;van Dam et al, 2017;Czislowski et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Comparison of Secreted in Xylem (SIX) genes in two fusarium wilt pathogens of ornamental palms

2019

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Fusarium oxysporum ff. sp. canariensis (Foc) and palmarum (Fop) cause lethal fusarium wilt on ornamental palms. Foc infects Phoenix canariensis and has a worldwide presence, whereas Fop primarily infects Washingtonia robusta and Syagrus romanzoffiana and is currently primarily restricted to Florida (USA). A Secreted in Xylem (SIX) gene profile was obtained for Fop and Foc isolates from the USA. SIX1, SIX7, SIX10 and SIX12 were detected in most Foc isolates and, with the exception of SIX12, with minimal sequence polymorphism. SIX8 and SIX9 were detected in all Fop isolates, with no sequence polymorphism. SIX10 was also present in seven of the Fop isolates. Phylogenetic trees were constructed using EF-1α‐, SIX1, SIX7 and SIX10 gene sequences from this study and previously derived sequences from Foc isolates obtained in Australia, the Canary Islands and Japan. The topology of the housekeeping EF‐1α gene indicated Foc is polyphyletic, with the Australian isolates separating into a distinct group from all other Foc isolates. However, the topologies of SIX1, SIX7 and SIX10 phylogenetic trees for Foc indicate monophyly. As has been proposed previously, this suggests the core genome of Foc evolved into a separate lineage after the SIX genes were conserved within the whole genome. This study is the first to generate SIX12 sequences for Foc. Interestingly, the topology of the SIX12 phylogenetic tree suggests polyphyly. For Fop, the topologies of the EF‐1α, SIX8 and SIX9 phylogenetic trees support monophyly. The distinct SIX gene profile and EF‐1α sequence of Fop demonstrates an independent evolutionary origin from Foc.

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A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species

Cited by 134 publications

References 62 publications

A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

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

Comparison of Secreted in Xylem (SIX) genes in two fusarium wilt pathogens of ornamental palms

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