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Comparative genomics of Fusarium oxysporum f. sp. melonis strains reveals nine lineages and a new sequence type of AvrFom2.

ABSTRACT: Fusarium oxysporum f. sp. melonis (Fom) is one of the most important pathogens of melon worldwide. In this study, we investigated the genomic diversity of Fom. One of the aims was to find clues for the origin(s) and dispersal of clonal lineages and races of Fom. We therefore included a large number of Fom strains from Iran, where melon has been cultivated for at least 5000 years. In 33 new genome sequences of Fom strains from different geographical regions of Iran and across the world, 40 new candidate effector genes were identified. Presence/absence of candidate effector genes and phylogenetic analyses resolved nine Fom lineages. The presence of a highly similar set of effector genes in some distant lineages is suggestive of horizontal chromosome transfer, a process known to occur in the Fusarium oxysporum species complex. Race 1.2, which breaks both Fom1 and Fom2 resistance genes, occurs in three of the nine lineages, two of which are predominant in Iran. We also identified a new sequence type of the AVRFom2 avirulence gene in one lineage. Expression of this sequence type during melon infection and genetic complementation suggest that this sequence type is not recognized by the Fom2 resistance protein.

SUBMITTER: Sabahi F

PROVIDER: S-EPMC8246983 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fusarium oxysporum f. sp. melonis Snyd. & Hans race 1.2 (FOM1.2) is the most virulent and yield-limiting pathogen of melon (Cucumis melo L.) worldwide. Current information suggest that the resistance to race 1.2 is controlled by multiple recessive genes and strongly affected by the environment. RNA-Seq analysis was used to identify candidate resistance genes and to dissect the early molecular processes deployed during melon-FOM1.2 interaction in the resistant doubled haploid line NAD and in the susceptible genotype Charentais-T (CHT) at 24 and 48 h post-inoculation (hpi). The transcriptome analysis of the NAD-FOM1.2 interaction identified 2,461 and 821 differentially expressed genes (DEGs) at 24 hpi and at 48 hpi, respectively, while in susceptible combination CHT-FOM1.2, 882 and 2,237 DEGs were recovered at 24 hpi and at 48 hpi, respectively. The overall expression profile suggests a prompt activation of the defense responses in NAD due to its basal defense-related machinery that allows an early pathogen recognition. Gene Ontology (GO) enrichment analyses revealed a total of 57 GO terms shared by both genotypes and consistent with response to fungal infection. GO classes named "chitinase activity," "cellulase activity," "defense response, incompatible interaction," "auxin polar transport" emerged as major factors of resistance to FOM1.2. The data indicated that NAD reacts to FOM1.2 with a fine regulation of Ca2+-mediated signaling pathways, cell wall reorganization, and hormone crosstalk (jasmonate and ethylene, auxin and abscissic acid). Several unannotated transcripts were recovered providing a basis for a further exploration of the melon resistance genes. DEGs belonging to the FOM1.2 genome were also detected in planta as a resource for the identification of potential pathogenicity factors. This work provides a broader view of the dynamic changes of the melon transcriptome triggered by FOM1.2 and highlights that the resistance response of NAD is mainly signaled by jasmonic acid and ethylene pathways mediated by ABA and auxin. The role of candidate plant and fungal responsive genes involved in the resistance is discussed.

Project description:The polyphyletic nature of many formae speciales of Fusarium oxysporum prevents 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 same forma 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-affecting formae speciales When tested on a collection of strains encompassing different clonal lineages of these formae speciales, nonpathogenic strains, and strains of other formae speciales, they allowed clear recognition of the host range of each evaluated strain. Within Fusarium oxysporum f. sp. melonis more genetic variability exists than anticipated, resulting in three F. oxysporum f. sp. melonis marker patterns that partially overlapped with the cucurbit-infecting Fusarium oxysporum f. sp. cucumerinum, Fusarium oxysporum f. sp. niveum, Fusarium oxysporum f. sp. momordicae, and/or Fusarium oxysporum f. sp. lagenariae For F. oxysporum f. 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 mentioned F. oxysporum pathogens. Additionally, the method can be applied to find markers distinguishing other host-specific forms of F. oxysporumIMPORTANCE Pathogenic strains of Fusarium oxysporum are differentiated into formae speciales based 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 these formae speciales This hinders accurate and rapid pathogen detection through molecular methods. In our research, we compared the genomes of 88 strains of F. oxysporum with each other, specifically targeting virulence-related genes that are typically highly similar within each forma specialis Using this approach, we identified marker sequences that allow the discrimination of F. oxysporum strains affecting various cucurbit plant species through different PCR-based methods.

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Comparative genomics of Fusarium oxysporum f. sp. melonis strains reveals nine lineages and a new sequence type of AvrFom2.

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