Apoplastic Venom Allergen-like Proteins of Cyst Nematodes Modulate the Activation of Basal Plant Innate Immunity by Cell Surface Receptors

Abstract

Despite causing considerable damage to host tissue during the onset of parasitism, nematodes establish remarkably persistent infections in both animals and plants. It is thought that an elaborate repertoire of effector proteins in nematode secretions suppresses damage-triggered immune responses of the host. However, the nature and mode of action of most immunomodulatory compounds in nematode secretions are not well understood. Here, we show that venom allergen-like proteins of plant-parasitic nematodes selectively suppress host immunity mediated by surface-localized immune receptors. Venom allergen-like proteins are uniquely conserved in secretions of all animal- and plant-parasitic nematodes studied to date, but their role during the onset of parasitism has thus far remained elusive. Knocking-down the expression of the venom allergen-like protein Gr-VAP1 severely hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and two other venom allergen-like proteins from the beet cyst nematode Heterodera schachtii in plants resulted in the loss of basal immunity to multiple unrelated pathogens. The modulation of basal immunity by ectopic venom allergen-like proteins in Arabidopsis thaliana involved extracellular protease-based host defenses and non-photochemical quenching in chloroplasts. Non-photochemical quenching regulates the initiation of the defense-related programmed cell death, the onset of which was commonly suppressed by venom allergen-like proteins from G. rostochiensis, H. schachtii, and the root-knot nematode Meloidogyne incognita. Surprisingly, these venom allergen-like proteins only affected the programmed cell death mediated by surface-localized immune receptors. Furthermore, the delivery of venom allergen-like proteins into host tissue coincides with the enzymatic breakdown of plant cell walls by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilize venom allergen-like proteins to suppress the activation of defenses by immunogenic breakdown products in damaged host tissue.

Plant pathogenesis–related proteins of the cacao fungal pathogen Moniliophthora perniciosa differ in their lipid-binding specificities

“…However, this protein is not essential for virulence on tomato (15). Gr-Vap1, a CAP protein from the potato cyst nematode Globodera rostochiensis, on the other hand, induces the loss of basal immunity to unrelated pathogens when heterologously expressed in plants (16). In addition, the knock-down of GrVap1 expression reduces the infectivity of nematode, indicating that this protein is important for pathogen-induced suppression of plant defense.…”

The barber's pole worm CAP protein superfamily — A basis for fundamental discovery and biotechnology advances

“…In addition, we propose that gender-enriched transcription profiles for Hc-cap-36 and Hc-cap-37 (females) or Hc-cap-38 (males) in haematophagous stages relate also to reproductive and/or developmental processes. A recent molecular investigation (Lozano-Torres et al, 2014) has shown that the silencing of a gene of Globodera rostochiensis (potato cyst nematode) with ~35% homology to Hc-cap-38 suppressed the activation of plant host defences, indicating a role of at least some CAP protein gene homologs in immune modulation.…”

Significant effects of RNAi silencing of the venom allergen‐like protein (Mhi‐vap‐1) of the root‐knot nematodeMeloidogyne hispanicain the early events of infection

“…Studies with G. rostochiensis showed that Gr‐VAP‐1 proteins suppress plant immunity and knockdown of this gene reduced nematode infection of potatoes (Lozano‐Torres et al ., ). In addition, it was shown that the vap‐1 gene is potentially associated with the induction of a host immune response and resistance because it triggers a Cf‐2/Rcr3pim‐dependent programmed cell death in tomato plants; it can also suppress the cell death caused by the extracellular receptor protein Cf‐4/Avr‐4, which is a cell surface immune receptor (Lozano‐Torres et al ., , ). Phylogenetic studies with the predicted protein sequences of VAP‐1 between M. hispanica and several other species of PPNs revealed a high degree of conservation (Duarte et al ., ).…”

“…Phylogenetic studies with the predicted protein sequences of VAP‐1 between M. hispanica and several other species of PPNs revealed a high degree of conservation (Duarte et al ., ). The Mi‐VAP‐1 shows about 28.6% of identity to Gr‐VAP‐1 (Lozano‐Torres et al ., ). Recently, the vap‐1 gene was localized, by in situ hybridization, in the subventral oesophageal gland cells of M. hispanica J2 and it was shown that tomato root exudates induce transcriptional changes of this gene in the pre‐parasitic J2, causing its up‐regulation even before nematodes penetrate the tomato roots (Duarte et al ., , ).…”

“…The VAP proteins, characterized by the highly conserved spacing of cysteine residues mainly in the carboxy‐terminal region (Hawdon et al ., ), are transcribed during plant–nematode parasitism. The vap genes were isolated in B. mucronatus , B. xylophilus , Ditylenchus africanus , G. rostochiensis , H. glycines , M. hispanica and M. incognita (Gao et al ., ; Wang et al ., ; Lozano‐Torres et al ., , ; Yan et al ., ; Duarte et al ., ). In B. xylophilus and B. mucronatus , six new VAPs were found, which were not homologous to known VAPs, and their functions still remain to be elucidated (Yan et al ., ).…”