Effector profiles distinguish <i>formae speciales</i> of <i>Fusarium oxysporum</i>

Dam, Peter van; Fokkens, Like; Schmidt, Sarah M.; Linmans, Jasper; Kistler, H. Corby; Li, Jun; Rep, Martijn

doi:10.1111/1462-2920.13445

Cited by 160 publications

(263 citation statements)

References 61 publications

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“…The effectors encoded on the pathogenicity chromosome are important determinants for pathogenicity and are under strict transcriptional regulation [26,46–50]. To determine whether transcription factors encoded on the pathogenicity chromosome can induce effector gene expression, strains ectopically expressing these transcription factors from a constitutive promoter—from hereon called ‘overexpressors’–were generated and tested for their ability to induce effector gene expression.…”

Section: Resultsmentioning

confidence: 99%

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Transcription Factors Encoded on Core and Accessory Chromosomes of Fusarium oxysporum Induce Expression of Effector Genes

et al. 2016

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Proteins secreted by pathogens during host colonization largely determine the outcome of pathogen-host interactions and are commonly called ‘effectors’. In fungal plant pathogens, coordinated transcriptional up-regulation of effector genes is a key feature of pathogenesis and effectors are often encoded in genomic regions with distinct repeat content, histone code and rate of evolution. In the tomato pathogen Fusarium oxysporum f. sp. lycopersici (Fol), effector genes reside on one of four accessory chromosomes, known as the ‘pathogenicity’ chromosome, which can be exchanged between strains through horizontal transfer. The three other accessory chromosomes in the Fol reference strain may also be important for virulence towards tomato. Expression of effector genes in Fol is highly up-regulated upon infection and requires Sge1, a transcription factor encoded on the core genome. Interestingly, the pathogenicity chromosome itself contains 13 predicted transcription factor genes and for all except one, there is a homolog on the core genome. We determined DNA binding specificity for nine transcription factors using oligonucleotide arrays. The binding sites for homologous transcription factors were highly similar, suggesting that extensive neofunctionalization of DNA binding specificity has not occurred. Several DNA binding sites are enriched on accessory chromosomes, and expression of FTF1, its core homolog FTF2 and SGE1 from a constitutive promoter can induce expression of effector genes. The DNA binding sites of only these three transcription factors are enriched among genes up-regulated during infection. We further show that Ftf1, Ftf2 and Sge1 can activate transcription from their binding sites in yeast. RNAseq analysis revealed that in strains with constitutive expression of FTF1, FTF2 or SGE1, expression of a similar set of plant-responsive genes on the pathogenicity chromosome is induced, including most effector genes. We conclude that the Fol pathogenicity chromosome may be partially transcriptionally autonomous, but there are also extensive transcriptional connections between core and accessory chromosomes.

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Section: Resultsmentioning

confidence: 99%

“…Blue bars: comparison between Fol4287 in planta and Fol4287 axenic cultures. The wild type strains Fol4287 and Fol007 are very similar [7,50]. One star (*): p<0.05, two stars (**): p<0.01.…”

Section: Resultsmentioning

confidence: 99%

Transcription Factors Encoded on Core and Accessory Chromosomes of Fusarium oxysporum Induce Expression of Effector Genes

et al. 2016

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“…erythroxili, suggesting that these isolates are closely related to FOL isolates of VCG0031. F. oxysporum isolates usually have a very narrow host range (45); hence, we assume that F. oxysporum f. sp. batatas and F. oxysporum f. sp.…”

Section: Resultsmentioning

confidence: 99%

“…batatas and F. oxysporum f. sp. erythroxili are pathogenic only on sweet potato and cocoa plant, respectively, and do not have the effector repertoire that is required for virulence on tomato and is encoded on chromosome 14 in FOL4287 (45).…”

Section: Resultsmentioning

confidence: 99%

“…This might be true at least for FOL, where a small chromosome, designated chromosome 14, has been shown to transfer between different isolates of F. oxysporum (46). The effector genes in FOL that facilitate virulence on tomato are located on chromosome 14 and are most likely absent from other formae speciales (42,45). The conservation of these genes with 100% identity in FOL isolates belonging to different clades suggests that pathogenicity toward cultivated tomato has spread relatively recently to different clades through horizontal chromosome transfer.…”

Section: Discussionmentioning

confidence: 99%

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Multiple Evolutionary Trajectories Have Led to the Emergence of Races in Fusarium oxysporum f. sp. lycopersici

Biju

Fokkens

Houterman

et al. 2017

Appl Environ Microbiol

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Race 1 isolates of Fusarium oxysporum f. sp. lycopersici (FOL) are characterized by the presence of AVR1 in their genomes. The product of this gene, Avr1, triggers resistance in tomato cultivars carrying resistance gene I. In FOL race 2 and race 3 isolates, AVR1 is absent, and hence they are virulent on tomato cultivars carrying I. In this study, we analyzed an approximately 100-kb genomic fragment containing the AVR1 locus of FOL race 1 isolate 004 (FOL004) and compared it to the sequenced genome of FOL race 2 isolate 4287 (FOL4287). A genomic fragment of 31 kb containing AVR1 was found to be missing in FOL4287. Further analysis suggests that race 2 evolved from race 1 by deletion of this 31-kb fragment due to a recombination event between two transposable elements bordering the fragment. A worldwide collection of 71 FOL isolates representing races 1, 2, and 3, all known vegetative compatibility groups (VCGs), and five continents was subjected to PCR analysis of the AVR1 locus, including the two bordering transposable elements. Based on phylogenetic analysis using the EF1-␣ gene, five evolutionary lineages for FOL that correlate well with VCGs were identified. More importantly, we show that FOL races evolved in a stepwise manner within each VCG by the loss of function of avirulence genes in a number of alternative ways.IMPORTANCE Plant-pathogenic microorganisms frequently mutate to overcome disease resistance genes that have been introduced in crops. For the fungus Fusarium oxysporum f. sp. lycopersici, the causal agent of Fusarium wilt in tomato, we have identified the nature of the mutations that have led to the overcoming of the I and I-2 resistance genes in all five known clonal lineages, which include a newly discovered lineage. Five different deletion events, at least several of which are caused by recombination between transposable elements, have led to loss of AVR1 and overcoming of I. Two new events affecting AVR2 that led to overcoming of I-2 have been identified. We propose a reconstruction of the evolution of races in FOL, in which the same mutations in AVR2 and AVR3 have occurred in different lineages and the FOL pathogenicity chromosome has been transferred to new lineages several times.

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Serial passage through resistant and susceptible cucumber cultivars affects the virulence of Fusarium oxysporum f. sp. cucumerinum

et al. 2018

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Fusarium oxysporum f. sp. cucumerinum (Foc) is the causal pathogen of cucumber Fusarium wilt resulting in losses to cucumber production. To investigate the effects of the selective pressures of host plants on the virulence of Foc, a low virulence isolate, foc-3b, was successively inoculated on resistant and susceptible cucumber cultivars for five generations. The virulence of the original isolate diverged; virulence was significantly strengthened after serial passage on the resistant cultivar and weakened on the susceptible plants (p ˂ .05). The expression of four virulence-related genes of F. oxysporum, G-protein α subunit gene fga1, sucrose nonfermenting 1 gene snf1, F-box protein gene frp1, and Class V chitin synthase gene chsV, was quantified using real-time PCR. All genes were significantly upregulated after serial passage on the resistant cultivar, compared to the original strain, and the expression of snf1 was downregulated in strains re-isolated from the susceptible plants (p ˂ .05). A significant positive correlation was found between the expression levels of gene snf1, frp1, and chsV and disease severity of cucumber Fusarium wilt, suggesting these genes may impact virulence differentiation. This study will improve the management of cucumber Fusarium wilt and provide insight into the mechanisms underlying virulence of F. oxysporum.

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Effector profiles distinguish formae speciales of Fusarium oxysporum

Cited by 160 publications

References 61 publications

Transcription Factors Encoded on Core and Accessory Chromosomes of Fusarium oxysporum Induce Expression of Effector Genes

Transcription Factors Encoded on Core and Accessory Chromosomes of Fusarium oxysporum Induce Expression of Effector Genes

Multiple Evolutionary Trajectories Have Led to the Emergence of Races in Fusarium oxysporum f. sp. lycopersici

Serial passage through resistant and susceptible cucumber cultivars affects the virulence of Fusarium oxysporum f. sp. cucumerinum

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