Apoplastic venom allergen-like proteins of plant-parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors

Despite causing considerable damage to host tissue during parasitism, nematodes establish persistent infections in both animals and plants. An elaborate repertoire of nematode effectors modulates damage-triggered immune responses of the host. However, the nature and mode of action of most of nematode immunomodulatory compounds is not well understood. We discovered that the nematode effectors named the venom allergen-like proteins (VAPs) selectively suppress host immunity during the onset of parasitism in plants. VAPs are uniquely conserved in secretions of all animal- and plant-parasitic nematodes, but their role in parasitism has remained elusive. Knocking-down the expression of Gr-VAP1 hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and VAPs from the beet cyst nematode Heterodera schachtii, in Arabidopsis, resulted in the loss of basal immunity to multiple pathogens. Surprisingly, VAPs only affect the defence responses mediated by surface-localised immune receptors. The modulation of basal immunity by ectopic expression of VAPs involves extracellular protease-based host defences and jasmonic acid responses. Crystal structures of VAPs revealed lipid binding motifs. In these cavities VAPs can bind palmitate and sterol both in vitro and in vivo. The delivery of VAPs into host tissue coincides with large modifications in the extracellular matrix by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilise VAPs to suppress the activation of defences by immunogenic breakdown products in damaged host tissue.