Cross-Kingdom Global Proteomics Reveals Specific Modulation of Disease Signaling in Multi-Host Fungal Pathogen Infection in Chickpea and Worm

An interconnected loop of messages and counter-messages determine the outcome of host-pathogen interactions. Multihost pathogenicity across plants and animals, particularly nematode, is a major source of new infectious diseases. <i>Fusarium oxysporum</i>, a multihost pathogen, causes vascular wilt in chickpea and fusariosis in worm and humans. To comprehend <i>Fusarium</i>-responsive multihost pathogenicity, we temporally profiled cross-kingdom species, chickpea and worm using SWATH-mass spectrometry. Morphological analyses revealed that increased wilting and intestinal disintegration elicits a disease response in chickpea and worm. Peptide-spectrum library consisted of 5629 and 3138 proteins from <i>Fusarium</i> infected chickpea and worm, respectively. SWATH analysis identified 1573 and 2249 disease-responsive chickpea (CaDRPs) and worm proteins (CeDRPs) linked to diverse organs, organelles, and functionality. Pairwise comparisons; over-representation analysis between time, treatment, and organism; wilt, and fusariosis diseasome revealed common and unique modules. CaDRPs involved in preformed defense, biomolecule synthesis, phytohormone regulation, ser/thr kinase, and ATP signaling have perturbed interactions and functions, majorly in chloroplast. CeDRPs linked to the cuticular support, muscle organization, neuronal information, intestinal metabolism, G-protein, and notch signaling showed a deregulated function, especially in the cytoplasm. Common biological processes, included primary metabolism, ribosome biogenesis, calcium signaling, and proteostasis. Our data provide first evidence of translational plasticity in the <i>Fusarium</i> diseasome providing novel insights into multihost pathogenesis.