Rhg1 -mediated selective autophagy degrades the nematode effector HgGID to increase soybean cyst nematode resistance

Abstract

Plant-parasitic nematodes are sophisticated metazoan pathogens that deploy complex, animal-like effector repertoires to manipulate host cellular machinery. The Rhg1 locus drives the primary resistance against soybean cyst nematode (Heterodera glycines), yet the mechanism by which its encoded atypical Soluble N-ethylmaleimide-sensitive factor Attachment Protein 18 (SNAP18) proteins restrict this evolutionarily advanced pathogen remains a long-standing enigma. Here, we reveal that Rhg1-mediated resistance operates as a suicide-bait strategy that converts a nematode virulence factor into a selective-autophagic trap. TurboID proximity labeling identified HgGID (glucose-induced degradation), a secreted nematode effector that physically associates with SNAP18 and co-enriches ubiquitin-proteasome components and SNARE-associated factors, consistent with a virulence strategy that engages host trafficking machinery during syncytium formation. Notably, the Rhg1-encoded atypical SNAP18 variant subverts this virulence strategy. We show that HgGID binds all 3 SNAP18 variants, whereas the resistance-associated SNAP18LC/HC variants favor increased dynamic accessibility of the HgGID AIM and promote its ATG8-dependent selective degradation. Ultimately, this targeted autophagic clearance efficiently neutralizes the virulence function of HgGID, establishing a novel paradigm for plant immunity against metazoan pathogens. Our findings uncover a molecular arms race where the host repurposes its vesicle transport machinery into an immune trap, highlighting the central role of selective autophagy in determining the outcome of host-metazoan interactions.