A nematode effector hijacks a host RBR-type E3 ubiquitin ligase to regulate NRC4 receptor-mediated plant immunity and facilitate parasitism

Abstract

The root-knot nematode Meloidogyne incognita is an obligate biotrophic pathogen that causes extensive losses to agriculture worldwide. Effectors secreted by the parasite play an essential role during nematode infection through suppressing plant innate immunity. Here, we identify and characterize a M. incognita effector designated as MiV86, which is secreted into plant cells and positively regulates nematode parasitism. We show that MiV86 interacts with RING finger protein 217 (NbRNF217), an RBR-type E3 ubiquitin ligase of Nicotiana benthamiana, which negatively regulates plant immunity in an enzymatic activity-dependent manner. Moreover, we demonstrate that NbRNF217 targets and ubiquitinates the helper nucleotide-binding leucine-rich repeat receptor protein NRC4, resulting in its relocation and degradation through the 26S proteasome and endosomal/vacuolar pathways. NbRNF217 regulates its homeostasis through self-catalyzed ubiquitination or external ubiquitination modifications, and we show that MiV86 inhibits the ubiquitination of NbRNF217 in planta without affecting its activity, thereby promoting the degradation of NRC4, which also contributes to the resistance of N. benthamiana against M. incognita. Our findings reveal a mechanism by which a nematode effector hijacks an E3 ubiquitin ligase to attenuate NRC4-mediated plant immunity, facilitating nematode parasitism.