Journal Article

The root‐knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism

Huang, Kaiwei, Quentin, Michaël, Jaubert, Stéphanie, Soulé, Salomé, Truong, Nhat My, Favery, Bruno, Bazin, Jérémie, Mulet, Karine, Kika, Junior Lusu, Mejias, Joffrey, Abad, Pierre, Zhao, Jianlong

2024

Overview

Root‐knot nematodes (RKNs) are microscopic parasitic worms able to infest the roots of thousands of plant species, causing massive crop yield losses worldwide. They evade the plant's immune system and manipulate plant cell physiology and metabolism to transform a few root cells into giant cells, which serve as feeding sites for the nematode. RKN parasitism is facilitated by the secretion in planta of effector molecules, mostly proteins that hijack host cellular processes. We describe here a conserved RKN‐specific effector, effector 12 (EFF12), that is synthesized exclusively in the oesophageal glands of the nematode, and we demonstrate its function in parasitism. In the plant, MiEFF12 localizes to the endoplasmic reticulum (ER). A combination of RNA‐sequencing analysis and immunity‐suppression bioassays revealed the contribution of MiEFF12 to the modulation of host immunity. Yeast two‐hybrid, split luciferase and co‐immunoprecipitation approaches identified an essential component of the ER quality control system, the Solanum lycopersicum plant bap‐like (PBL), and basic leucine zipper 60 (BZIP60) proteins as host targets of MiEFF12. Finally, silencing the PBL genes in Nicotiana benthamiana decreased susceptibility to Meloidogyne incognita infection. Our results suggest that EFF12 manipulates PBL function to modify plant immune responses to allow parasitism. The Meloidogyne incognita effector MiEFF12 targets endoplasmic reticulum‐resident proteins and corrupts their function in the host immune response to promote parasitism.

• Publisher: John Wiley & Sons, Inc,Wiley,John Wiley and Sons Inc
• Subject: Bioassays / Biosynthesis / Cell death / cell physiology / Control systems / Crop yield / effector / Effector cells / Endoplasmic reticulum / endoplasmic reticulum (ER) / ER quality control / Gene sequencing / Gene silencing / Genes / Genetic engineering / Giant cells / Host plants / Hybrid systems / Immune response / Immune system / immunity / Immunoprecipitation / Leucine / leucine zipper / Leucine zipper proteins / Life Sciences / luciferase / Meloidogyne incognita / metabolism / Nematodes / Nicotiana benthamiana / Original / Parasites / Parasitism / Pathogens / Peptides / Phylogenetics / Plant cells / Plant immunity / plant pathology / Plant species / precipitin tests / Proteins / Quality control / Root knot / root-knot nematodes / secretion / Sequence analysis / Solanum lycopersicum / species / two hybrid system techniques / Yeast