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

PLoS Pathogens

Aska Goverse¹  Geert Smant¹  Jose L. Lozano-Torres²  Anna Finkers-Tomczak²  Amalia Diaz-Granados²  Johannes Helder²  Ruud H. P.Wilbers²  Casper C. van Schaik²  Jaap Bakker²  Sonja Warmerdam²  Arjen Schots² 

[1] Centre for BioSystems Genomics, Wageningen, The Netherlands;Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands

关键词: Arabidopsis thaliana;    Genetically modified plants;    Venoms;    Nematode infections;    Plant disease resistance;    Tomatoes;    Cysteine proteases;    Potato;   

DOI  :  10.1371/journal.ppat.1004569

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY