Large-scale protein interactome reveals lineage-specific genes driving plant-parasitic nematode adaptive innovations

Mounting evidence suggests that lineage-specific genes drive phenotype diversity. Plant-parasitic nematodes (PPNs), among the most destructive plant pathogens, have evolved innovated traits required for plant parasitism, yet the genetic basis remains unclear. Here, we identify PPN lineage-specific genes (PPNLSGs) and analyze the large-scale protein interactome of their encoded proteins (PPNLSPs). By using yeast two-hybrid assays, we identify 2705 protein-protein interactions involving PPNLSPs from stem nematode Ditylenchus destructor, and by using computational methods, we predict conserved interactions of D. destructor proteins at the genome-wide level. Integration of these data allows generating a comprehensive protein interactome map, showing established complexes and PPNLSP modules, and allowing functional annotations for 306 uncharacterized PPNLSPs. Among these interactions, we identify multiple PPNLSPs associated with chemotaxis and infectivity based on these PPNLSP modules and propose a chemotaxis pathway model of host seeking. Our study indicates PPNLSGs as drivers of PPN adaptive innovations and provides a reference resource for future research on PPN biology and control strategies.