A key virulence effector from cyst nematodes targets host autophagy to promote nematode parasitism

Authors: CHEN, JIANSONG - Cornell University; CHEN, SHIYAN - Cornell University; XU, CHUNLING - Cornell University; Yang, Huijun; ACHOM, MINGKEE - Cornell University; Wang, Xiaohong

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2023
Publication Date: 11/8/2023
Citation: Chen, J., Chen, S., Xu, C., Yang, H., Achom, M., Wang, X. 2023. A key virulence effector from cyst nematodes targets host autophagy to promote nematode parasitism. New Phytologist. 237:1374-1390. https://doi.org/10.1111/nph.18609.
DOI: https://doi.org/10.1111/nph.18609

Interpretive Summary: Cyst nematodes are devastating plant pests that can cause significant crop yield losses. These root parasites secrete proteins, called effectors, into root cells to enable successful infection. However, the identity and function of most nematode-secreted effectors are largely unknown. In this study, we identified a novel effector gene named PIMP4 present in major cyst nematode species. We used multiple approaches to demonstrate that PIMP4 effectors function to suppress plant defenses to aid nematode infection. We further discovered that PIMP4 effectors contain a conserved sequence that targets components of autophagy, a major protein degradation system in eukaryotes that has been recently linked to plant defenses. This study revealed for the first time that cyst nematodes have evolved effectors to target the host autophagy system to induce disease. Given the importance of PIMP4 effectors in nematode parasitism, disruption of PIMP4 through a plant-delivered RNA interference approach may result in nematode resistance in crop plants.

Technical Abstract: Cyst nematodes (Heterodera and Globodera spp.) are obligate root parasites that secrete effector proteins into host cells to modulate various cellular responses to achieve infection. However, the identity and function of most nematode effectors are largely unknown. We report here the identification of a novel effector PIMP4 (Plant Immunity Manipulating Protein 4), found to be broadly conserved in cyst nematode species. We used molecular and genetic analyses to demonstrate that PIMP4 is important for nematode parasitism. PIMP4 effectors are potent in suppressing ROS induced by flg22 and cell-death mediated by immune receptors in Nicotiana benthamiana, revealing a key role of PIMP4 in virulence. ATG8 (AuTophaGy-related protein 8) is a central component of autophagy, a major protein degradation process in eukaryotes that has been linked to plant immunity. PIMP4 effectors were predicted to contain two AIM (ATG8-Interacting Motif) sequences. GrPIMP4 from G. rostochiensis specifically interacts with the potato (Solanum tuberosum) ATG8-1.1 protein (StATG8-1.1) demonstrated via in planta protein-protein interaction assays. Mutation in AIM2 of GrPIMP4 abolishes its interaction with StATG8-1.1 and its activity in ROS suppression. Collectively, our results uncover a unique mechanism by which cyst nematodes employ a key virulence and AIM-containing effector to perturb host autophagy to promote disease.