The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

Abstract

Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with Arabidopsis GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.

Effectors of Root-Knot Nematodes: An Arsenal for Successful Parasitism

“…EFF-1, a nuclear localized effector is expressed in J3/J4 and females of M. incognita and present in multiple RKN species ( Jaouannet et al, 2012 ). In the GC nucleus, it interacts with three plant proteins namely HUB-6, glyceraldehyde 3-phosphate dehydrogenase (GAPDH), and universal stress protein (USP; Godinho Mendes et al, 2021b ; Truong et al, 2021 ; Figure 4B ). HUB-6 is an important transcription factor that regulates the cell cycle, plant development, and plant immune response ( Li, 2015 ).…”

“…It is known that cytoplasmic GAPDH re-localizes to the nucleus under oxidative stress and protects nucleic acids. The ROS response generated during RKN infection could target GAPDH to GC nuclei and the interaction of EFF-1 with GAPDH suggests an alteration in its nuclear function of nucleic acid protection ( Truong et al, 2021 ). USP is a multifunctional protein involved in biotic and abiotic stress responses and in the nucleus, it binds to RNA to protect it during environmental stress ( Chi et al, 2019 ).…”

“…USP is a multifunctional protein involved in biotic and abiotic stress responses and in the nucleus, it binds to RNA to protect it during environmental stress ( Chi et al, 2019 ). EFF-1-USP interaction in the nucleus suggests that it affects the RNA-protective function of USP which may facilitate transcriptional modulation in GCs ( Truong et al, 2021 ). Further transcriptomic study identified another effector localized to the GC nuclei, namely a small glycine cysteine-rich-1 ( Table 2 ).…”

A secreted ribonuclease effector from Verticillium dahliae localizes in the plant nucleus to modulate host immunity

“…Functional analysis of nuclear effectors from other pathogens during their interactions with hosts have been reported. The Meloidogyne incognita nuclear effector MiEFF1 interacts with Arabidopsis thaliana cytoplasmic glyceraldehyde‐3‐phosphate dehydrogenase and promotes parasitism in A. thaliana (Truong et al, 2021). The effector MiSSP7 from the ectomycorrhizal fungus Laccaria bicolor localizes to the plant nucleus and interacts with PtJAZ6, a negative regulator of jasmonic acid (JA)‐induced gene regulation in Populus trichocarpa .…”

Characterization of Five Meloidogyne incognita Effectors Associated with PsoRPM3

“…MiEFF18 modulates SmD1 to facilitate giant cell formation [29]. Effector MiEFF1 targets cytosolic glyceraldehyde-3phosphate dehydrogenases (GAPCs) that are induced in giant cells, and their nonmetabolic functions are required for root-knot nematode infection [30]. In addition, some M. incognita effectors can promote relative invasion and parasitism by specifically interfering with functional proteins involved in plant defence, such as the effectors MiMIF-2, MiISE6, and Minc17998 [31][32][33].…”