Venom allergen-like proteins secreted by plant-parasitic nematodes modulate defense responses mediated by extracellular innate immune receptors

Plants and animals utilize cell-surface receptors to survey their direct environment for molecular patterns uniquely associated with infections by microbial invaders. Recently, we showed that a venom allergen-like protein Gr-VAP1 from the plant-parasitic nematode Globodera rostochiensis targets the papain-like cysteine protease Rcr3pim that functions as a cofactor of the extracellular plant immune receptor Cf-2 in tomato. However, the presence of Rcr3pim alone almost doubles the susceptibility of tomato plants to G. rostochiensis, suggesting that Gr-VAP1 modulates the activity of Rcr3pim to enhance the virulence of the nematodes. Although secreted venom allergen-like proteins are highly conserved among plant-parasitic nematodes, their function in parasitism of host plants is largely unknown. Here we demonstrate that venom allergen-like proteins from plant-parasitic nematodes specifically alter defense responses mediated by extracellular innate immune receptors. Knocking-down the expression of venom allergen-like proteins in G. rostochiensis strongly reduced the virulence of the nematodes. Ectopic expression of different venom allergen-like proteins from plant-parasitic nematodes in transgenic Arabidopsis plants significantly reduced their basal defense responses to nematodes, multiple other plant pathogens, and the immunogenic peptide flg22 from bacterial flagella. Furthermore, venom allergen-like proteins altered the defense-related programmed cell death activated by multiple extracellular plant immune receptors in leaves of Nicotiana benthamiana. We therefore propose that venom allergen-like proteins modulate the activation and/or signaling by extracellular immune receptors.