Background: F. oxysporum as a species complex (FOSC) possess the capacity, to specialize into host-specific pathogens deriving into formae speciales. This with the help of horizontal gene transfer (HGT) between pathogenic and endophytic individuals of FOSC. From these pathogenic forma speciales, F. oxysporum f. sp. vanillae (Fov) is the causal agent of fusarium wilt producing root and stem rot (RSR) positions itself was the main phytosanitary problem in vanilla plantations worldwide. Nonetheless, the origin of this forma specialis and the behavioral genetics dictating the endophytic/pathogenic Fusarium lifestyles are still unknown. To elucidate the underlying molecular mechanisms that establish these behaviors we analyzed the RNA-seq libraries of two-times frames of vanilla-fov interactions. Results: Our analyses identified the sets of transcripts corresponding to Fov pathogenic strain JAGH3 during the two-times frames of the infection as the sets of the transcripts belonging to endophytic Fox in vanilla. Functional predictions of de novo annotated transcripts as the enriched GO terms with the overrepresented metabolic pathways associated to them allowed us to identify the molecular processes that establish the pathogenic lifestyle in Fov being virulence, hypervirulence, sporulation, conidiation, necrosis and fusaric acid related genes with the carbohydrates, amino acids and proteins, glycerophospholipids and autophagy metabolic pathways that are key regulators of spores germination and pathogenicity establishment as the underlying mechanisms behind this behavior. As the absence of these were found in the vanilla endophytic Fox. Conclusions: This work reveals the main players of the behavioral genetics in pathogenic Fov/endophytic Fox in V. planifolia Jacks. Its pathogenic strategy allows Fov to infect in a SIX genes-independent manner. As the other pathogenic elements found in this study could be explained by the presence of pathogenicity islands and genomic regions associated with supernumerary chromosomes in Fov. These play a central role as carriers of genes involved with pathogenic activity and can be obtained through HGT.

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.