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Wilt disease affecting pomegranate crops results in rapid soil-nutrient depletion, reduced or complete loss in yield, and crop destruction. There are limited studies on the phytopathogen Fusarium oxysporum prevalence and associated genomic information with respect to Fusarium wilt in pomegranate. In this study, soil samples from the rhizosphere of different pomegranate plants showing early stage symptoms of wilt infection to an advanced stage were collected from an orchard situated in Karnataka, India. A whole metagenome sequencing approach was employed to gain insights into the adaptations of the causative pathogen F. oxysporum. Physicochemical results showed a drop in the pH levels, N, Fe, and Mn, and increase in electrical conductivity, B, Zn, Cl, Cu was observed in the early and intermediate stage samples. Comparative abundance analysis of the experimental samples ESI and ISI revealed an abundance of Proteobacteria phyla Achromobacter sp. 2789STDY5608625, Achromobacter sp. K91, and Achromobacter aegrifaciens and Eukaryota namely Aspergillus arachidicola, Aspergillus candidus, and Aspergillus campestris. Functional pathway predictions implied carbohydrate binding to be significant (p < 0.05) among the three experimental samples. Microbiological examination and whole microbiome analysis confirmed the prevalence of F. oxysporum in the soil samples. Variant analysis of F. oxysporum revealed multiple mutations in the 3IPD gene with high impact effects. 3-Isopropylmalate dehydratase and carbohydrate-active enzymes could be good targets for the development of antifungals that could aid in biocontrol of F. oxysporum. The present study demonstrates the capabilities of the whole metagenome sequencing approach for rapid identification of potential key players of wilt disease pathogenesis wherein the symptomatology is complex.

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