Cross-kingdom global proteomics reveals specific modulation of disease signaling in multi-host fungal pathogen infection in chickpea and worm

Abstract

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. Fusarium oxysporum, a multihost pathogen, causes vascular wilt in chickpea and fusariosis in worm and humans. To comprehend Fusarium-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 Fusarium 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 Fusarium diseasome providing novel insights into multihost pathogenesis.