Evidence for horizontal gene transfer and separation of effector recognition from effector function revealed by analysis of effector genes shared between cape gooseberry- and tomato-infecting formae speciales of Fusarium oxysporum

Members of the Fusarium oxysporum species complex (FOSC) has the capacity to specialize into host-specific pathogens known as formae speciales through horizontal gene transfer between pathogenic and endophytic individuals. To this day, the origin of these formae speciales and the genetic determinants dictating the switch from endophytic to pathogenic Fusarium oxysporum (Fox) are still unknown. F. oxysporum f. sp. vanillae (Fov), member of FOSC, is the causal agent of root and stem rot disease, representing the main phytosanitary problem in vanilla plantations worldwide. Here we analyzed the RNA-seq libraries resulting from the interaction vanilla-Fov at early and late stages of the infection, and what we initially identified as control in a previous study, detecting the presence of Fox endophytes. We identified virulence, hypervirulence, sporulation, conidiation, necrosis, and production of fusaric acid as key processes taking place during Fov-vanilla interaction. Through comparison with endophytic Fox, we found that Fov can infect vanilla thanks to the presence of pathogenicity islands and genomic regions associated with supernumerary chromosomes. These play a central role as carriers of genes involved with pathogenic activity and could have being obtained by Fov through horizontal gene transfer. We also found that, unlike other pathogenic members of FOSC, Fov do not use Secreted in Xylem proteins (SIX) to infect vanilla.

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Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation

10.1101/122499 ◽

2017 ◽

Author(s):

Jacob Thomas ◽

Samit S. Watve ◽

William C. Ratcliff ◽

Brian K. Hammer

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Horizontal Transfer ◽

Direct Injection ◽

Spatially Explicit ◽

Type Vi Secretion System ◽

Effector Genes ◽

Type Vi Secretion ◽

A Cell ◽

Explicit Simulation

AbstractHorizontal gene transfer can have profound effects on bacterial evolution by allowing individuals to rapidly acquire adaptive traits that shape their strategies for competition. One strategy for intermicrobial antagonism often used by Proteobacteria is the genetically-encoded contact-dependent Type VI secretion system (T6SS); a weapon used to kill heteroclonal neighbors by direct injection of toxic effectors. Here, we experimentally demonstrate thatVibrio choleraecan acquire new T6SS effector genes via horizontal transfer and utilize them to kill neighboring cells. Replacement of one or more parental alleles with novel effectors allows the recombinant strain to dramatically outcompete its parent. Through spatially-explicit simulation modeling, we show that the HGT is risky: transformation brings a cell into conflict with its former clonemates, but can be adaptive when superior T6SS alleles are acquired. More generally, we find that these costs and benefits are not symmetric, and that high rates of HGT can act as hedge against competitors with unpredictable T6SS efficacy. We conclude that antagonism and horizontal transfer drive successive rounds of weapons-optimization and selective sweeps, dynamically shaping the composition of microbial communities.

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Genetic Diversity in FUB Genes of Fusarium oxysporum f. sp. cubense Suggests Horizontal Gene Transfer

Frontiers in Plant Science ◽

10.3389/fpls.2019.01069 ◽

2019 ◽

Vol 10 ◽

Cited By ~ 1

Author(s):

Siwen Liu ◽

Bo Wu ◽

Shuxia Lv ◽

Zongzhuan Shen ◽

Rong Li ◽

...

Keyword(s):

Genetic Diversity ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Fusarium Oxysporum

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Putative Novel Effector Genes Revealed by the Genomic Analysis of the Phytopathogenic Fungus Fusarium oxysporum f. sp. physali (Foph) That Infects Cape Gooseberry Plants

Frontiers in Microbiology ◽

10.3389/fmicb.2020.593915 ◽

2021 ◽

Vol 11 ◽

Author(s):

Jaime Simbaqueba ◽

Edwin A. Rodríguez ◽

Diana Burbano-David ◽

Carolina González ◽

Alejandro Caro-Quintero

Keyword(s):

Fusarium Oxysporum ◽

Virulent Strain ◽

Management Strategies ◽

Genomic Analysis ◽

Single Copy ◽

Wilt Disease ◽

Limiting Factors ◽

Phytopathogenic Fungus ◽

Effector Genes ◽

Cape Gooseberry

The vascular wilt disease caused by the fungus Fusarium oxysporum f. sp. physali (Foph) is one of the most limiting factors for the production and export of cape gooseberry (Physalis peruviana) in Colombia. A transcriptomic analysis of a highly virulent strain of F. oxysporum in cape gooseberry plants, revealed the presence of secreted in the xylem (SIX) effector genes, known to be involved in the pathogenicity of other formae speciales (ff. spp.) of F. oxysporum. This pathogenic strain was classified as a new f. sp. named Foph, due to its specificity for cape gooseberry hosts. Here, we sequenced and assembled the genome of five strains of F. oxysporum from a fungal collection associated to the cape gooseberry crop (including Foph), focusing on the validation of the presence of SIX homologous and on the identification of putative effectors unique to Foph. By comparative and phylogenomic analyses based on single-copy orthologous, we found that Foph is closely related to F. oxysporum ff. spp., associated with solanaceous hosts. We confirmed the presence of highly identical homologous genomic regions between Foph and Fol that contain effector genes and identified six new putative effector genes, specific to Foph pathogenic strains. We also conducted a molecular characterization using this set of putative novel effectors in a panel of 36 additional stains of F. oxysporum including two of the four sequenced strains, from the fungal collection mentioned above. These results suggest the polyphyletic origin of Foph and the putative independent acquisition of new candidate effectors in different clades of related strains. The novel effector candidates identified in this genomic analysis, represent new sources involved in the interaction between Foph and cape gooseberry, that could be implemented to develop appropriate management strategies of the wilt disease caused by Foph in the cape gooseberry crop.

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Novel effector genes revealed by the genomic analysis of the phytopathogenic fungus Fusarium oxysporum f. sp. physali (Foph) that infects cape gooseberry plants

10.1101/2020.08.10.235309 ◽

2020 ◽

Author(s):

Jaime Simbaqueba ◽

Edwin A. Rodriguez ◽

Diana Burbano-David ◽

Carolina Gonzalez ◽

Alejandro Caro-Quintero

Keyword(s):

Fusarium Oxysporum ◽

Virulent Strain ◽

Management Strategies ◽

Genomic Analysis ◽

Illumina Miseq ◽

Wilt Disease ◽

Limiting Factors ◽

Phytopathogenic Fungus ◽

Effector Genes ◽

Cape Gooseberry

AbstractThe vascular wilt disease caused by the fungus Fusarium oxysporum f. sp. physali (Foph) is one of the most limiting factors for the production and export of cape gooseberry (Physalis peruviana) in Colombia. A previous study of the transcriptomic profile of a highly virulent strain of F. oxysporum in cape gooseberry plants, from a collection of 136 fungal isolates obtained from wilted cape gooseberry plants, revealed the presence of secreted in the xylem (SIX) effector genes, known to be involved in the pathogenicity of other F. oxysporum formae speciales (ff. spp.). This pathogenic strain was named Foph, due to its specificity for cape gooseberry hosts. Here, we sequenced the genome of Foph, using the Illumina MiSeq platform. We analyzed the assembled genome, focusing on the confirmation of the presence of homologues of SIX effectors and the identification of novel candidates of effector genes unique of Foph. By comparative and phylogenomic analyses based on single-copy orthologues, we identified that Foph is closely related to F. oxysporum ff. spp., associated with solanaceous hosts. We confirmed the presence of highly identical homologous genomic regions between Foph and Fol, that contain effector genes and identified seven new effector gene candidates, specific to Foph strains. We also conducted a molecular characterization of a panel of 29 F. oxysporum additional stains associated to cape gooseberry crops isolated from different regions of Colombia. These results suggest the polyphyletic origin of Foph and the putative independent acquisition of new candidate effectors in different clades of related strains. The novel effector candidates identified by sequencing and analyzing the genome of Foph, represent new sources involved in the interaction between Foph and cape gooseberry. These resources could be implemented to develop appropriate management strategies of the wilt disease caused by Foph in the cape gooseberry crop.

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Use of Comparative Genomics-Based Markers for Discrimination of Host Specificity in Fusarium oxysporum

Applied and Environmental Microbiology ◽

10.1128/aem.01868-17 ◽

2017 ◽

Vol 84 (1) ◽

Cited By ~ 20

Author(s):

Peter van Dam ◽

Mara de Sain ◽

Anneliek ter Horst ◽

Michelle van der Gragt ◽

Martijn Rep

Keyword(s):

Fusarium Oxysporum ◽

Host Range ◽

Host Specificity ◽

Plant Species ◽

Detection Methods ◽

Taqman Assay ◽

Content Type ◽

Formae Speciales ◽

Effector Genes ◽

Forma Specialis

ABSTRACTThe polyphyletic nature of manyformae specialesofFusarium oxysporumprevents molecular identification of newly encountered strains based on conserved, vertically inherited genes. Alternative molecular detection methods that could replace labor- and time-intensive disease assays are therefore highly desired. Effectors are functional elements in the pathogen-host interaction and have been found to show very limited sequence diversity between strains of the sameforma specialis, which makes them potential markers for host-specific pathogenicity. We therefore compared candidate effector genes extracted from 60 existing and 22 newly generated genome assemblies, specifically targeting strains affecting cucurbit plant species. Based on these candidate effector genes, a total of 18 PCR primer pairs were designed to discriminate between each of the seven Cucurbitaceae-affectingformae speciales. When tested on a collection of strains encompassing different clonal lineages of theseformae speciales, nonpathogenic strains, and strains of otherformae speciales, they allowed clear recognition of the host range of each evaluated strain. WithinFusarium oxysporumf. sp.melonismore genetic variability exists than anticipated, resulting in threeF. oxysporumf. sp.melonismarker patterns that partially overlapped with the cucurbit-infectingFusarium oxysporumf. sp.cucumerinum,Fusarium oxysporumf. sp.niveum,Fusarium oxysporumf. sp.momordicae, and/orFusarium oxysporumf. sp.lagenariae. ForF. oxysporumf. sp.niveum, a multiplex TaqMan assay was evaluated and was shown to allow quantitative and specific detection of template DNA quantities as low as 2.5 pg. These results provide ready-to-use marker sequences for the mentionedF. oxysporumpathogens. Additionally, the method can be applied to find markers distinguishing other host-specific forms ofF. oxysporum.IMPORTANCEPathogenic strains ofFusarium oxysporumare differentiated intoformae specialesbased on their host range, which is normally restricted to only one or a few plant species. However, horizontal gene transfer between strains in the species complex has resulted in a polyphyletic origin of host specificity in many of theseformae speciales. This hinders accurate and rapid pathogen detection through molecular methods. In our research, we compared the genomes of 88 strains ofF. oxysporumwith each other, specifically targeting virulence-related genes that are typically highly similar within eachforma specialis. Using this approach, we identified marker sequences that allow the discrimination ofF. oxysporumstrains affecting various cucurbit plant species through different PCR-based methods.

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