A pair of effectors encoded on a conditionally dispensable chromosome of<i>Fusarium oxysporum</i>suppress host-specific immunity

Ayukawa, Yu; Asai, Shuji; Gan, Pamela; Tsushima, Ayako; Ichihashi, Yasunori; Shibata, Arisa; Komatsu, Ken; Houterman, Petra M.; Rep, Martijn; Shirasu, Ken; Arie, Tsutomu

doi:10.1101/2020.10.06.329052

Cited by 5 publications

(14 citation statements)

References 74 publications

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“…Fol SIX3 (Avr2) and SIX5 are adjacent, divergently-transcribed genes with a common promoter and SIX5 has been shown to interact with SIX3 to promote virulence by enabling symplastic movement of SIX3 via plasmodesmata [17]. Focn SIX8 and PSE1 (pair with SIX8 1) are another such divergently-transcribed effector gene pair that function together to suppress phytoalexin production and plant immunity in Arabidopsis [18]. In Fol, SIX8 forms a similar gene pair with PSL1 (PSE1-like 1) [18].…”

Section: Introductionmentioning

confidence: 99%

“…Focn SIX8 and PSE1 (pair with SIX8 1) are another such divergently-transcribed effector gene pair that function together to suppress phytoalexin production and plant immunity in Arabidopsis [18]. In Fol, SIX8 forms a similar gene pair with PSL1 (PSE1-like 1) [18]. Despite their roles in fungal pathogenicity, the virulence functions of most SIX effectors remain unknown.…”

Section: Introductionmentioning

confidence: 99%

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The structural repertoire ofFusarium oxysporumf. sp.lycopersicieffectors revealed by experimental and computational studies

Outram

Smith

et al. 2021

Preprint

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Plant pathogens secrete proteins, known as effectors, that function in the apoplast and inside plant cells to promote virulence. Effectors can also be detected by cell-surface and cytosolic receptors, resulting in the activation of defence pathways and plant immunity. Our understanding of fungal effector function and detection by immunity receptors is limited largely due to high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. Recent studies have demonstrated that fungal effectors can be grouped into structural classes despite significant sequence variation. Using protein x-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class. Using AlphaFold ab initio protein structure prediction, benchmarked against the experimentally determined structures, we demonstrate SIX6 and SIX13 are FOLD effectors. We show that the conserved N-domain of Avr1 and Avr3 is sufficient for recognition by their corresponding, but structurally-distinct, immunity receptors. Additional structural prediction and comparison indicate that 11 of the 14 SIX effectors group into four structural families. This revealed that genetically linked effectors are related structurally, and we provide direct evidence for a physical association between one divergently-transcribed effector pair. Collectively, these data indicate that Fol secretes groups of structurally-related molecules during plant infection, an observation that has broad implications for our understanding of pathogen virulence and the engineering of plant immunity receptors.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The structural repertoire ofFusarium oxysporumf. sp.lycopersicieffectors revealed by experimental and computational studies

Outram

Smith

et al. 2021

Preprint

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“…Like SIX1 , SIX8 is also required for virulence of Focub TR4 on Cavendish banana ( An et al, 2019 ). Similarly, SIX8 is involved in conferring virulence to Fo-5176 on Arabidopsis and cabbage plants ( Ayukawa et al, 2020 ).…”

Section: Pathogenicity Factorsmentioning

confidence: 99%

“…These genes reside as a minicluster on chromosome 14 and their expression is under the control of the same bidirectional promoter present on the shared upstream region ( Schmidt et al, 2013 ). Another pair of effector genes, SIX8 – PSE1 , was identified in isolates capable of infecting Arabidopsis , and this pair was found to be associated with suppression of resistance in Arabidopsis ( Ayukawa et al, 2020 ). The mode of action of SIX8–PSE1 potentially involves suppression of a phytoalexin called camalexin.…”

Section: Pathogenicity Factorsmentioning

confidence: 99%

“…However, unlike SIX3 – SIX5 , no direct interaction between SIX8 – PSE1 was detected in yeast two-hybrid assays. Mutation in PSE1 , and not the SIX8 gene, resulted in evasion of recognition by the corresponding resistance protein suggesting that PSE1 is required to avoid detection ( Ayukawa et al, 2020 ). A conserved gene cluster SIX7/SIX10/SIX12 was also observed in formae speciales narcissi and gladioli ( Simbaqueba et al, 2018 ).…”

Section: Pathogenicity Factorsmentioning

confidence: 99%

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Secreted in Xylem Genes: Drivers of Host Adaptation in Fusarium oxysporum

et al. 2021

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Fusarium oxysporum (Fo) is a notorious pathogen that significantly contributes to yield losses in crops of high economic status. It is responsible for vascular wilt characterized by the browning of conductive tissue, wilting, and plant death. Individual strains of Fo are host specific (formae speciales), and approximately, 150 forms have been documented so far. The pathogen secretes small effector proteins in the xylem, termed as Secreted in Xylem (Six), that contribute to its virulence. Most of these proteins contain cysteine residues in even numbers. These proteins are encoded by SIX genes that reside on mobile pathogenicity chromosomes. So far, 14 proteins have been reported. However, formae speciales vary in SIX protein profile and their respective gene sequence. Thus, SIX genes have been employed as ideal markers for pathogen identification. Acquisition of SIX-encoding mobile pathogenicity chromosomes by non-pathogenic lines, through horizontal transfer, results in the evolution of new virulent lines. Recently, some SIX genes present on these pathogenicity chromosomes have been shown to be involved in defining variation in host specificity among formae speciales. Along these lines, the review entails the variability (formae speciales, races, and vegetative compatibility groups) and evolutionary relationships among members of F. oxysporum species complex (FOSC). It provides updated information on the diversity, structure, regulation, and (a)virulence functions of SIX genes. The improved understanding of roles of SIX in variability and virulence of Fo has significant implication in establishment of molecular framework and techniques for disease management. Finally, the review identifies the gaps in current knowledge and provides insights into potential research landscapes that can be explored to strengthen the understanding of functions of SIX genes.

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Genome editing using a versatile vector-based CRISPR/Cas9 system in Fusarium species

Shinkado

Saito

Yamazaki

et al. 2022

Sci Rep

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Fusarium species include important filamentous fungal pathogens that can infect plants, animals, and humans. Meanwhile, some nonpathogenic Fusarium species are promising biocontrol agents against plant pathogens. Here, we developed a genome editing technology using a vector-based CRISPR/Cas9 system for Fusarium oxysporum f. sp. lycopersici (Fol). This optimized CRISPR/Cas9 system, harboring an endogenous U6 small nuclear RNA promoter for the expression of single-guide RNA and an endogenous H2B nuclear localization signal for the localization of Cas9, enabled efficient targeted gene knock-out, including in the accessory chromosomal regions in Fol. We further demonstrated single crossover-mediated targeted base editing and endogenous gene tagging. This system was also applicable for genome editing in F. oxysporum f. sp. spinaciae and F. commune without any modifications, suggesting that this CRISPR/Cas9 vector has a potential application for a broad range of researches on other Fusarium species.

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A pair of effectors encoded on a conditionally dispensable chromosome ofFusarium oxysporumsuppress host-specific immunity

Cited by 5 publications

References 74 publications

The structural repertoire ofFusarium oxysporumf. sp.lycopersicieffectors revealed by experimental and computational studies

The structural repertoire ofFusarium oxysporumf. sp.lycopersicieffectors revealed by experimental and computational studies

Secreted in Xylem Genes: Drivers of Host Adaptation in Fusarium oxysporum

Genome editing using a versatile vector-based CRISPR/Cas9 system in Fusarium species

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