A novel Meloidogyne graminicola effector, MgGPP, is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism

Abstract

Plant pathogen effectors can recruit the host post-translational machinery to mediate their post-translational modification (PTM) and regulate their activity to facilitate parasitism, but few studies have focused on this phenomenon in the field of plant-parasitic nematodes. In this study, we show that the plant-parasitic nematode Meloidogyne graminicola has evolved a novel effector, MgGPP, that is exclusively expressed within the nematode subventral esophageal gland cells and up-regulated in the early parasitic stage of M. graminicola. The effector MgGPP plays a role in nematode parasitism. Transgenic rice lines expressing MgGPP become significantly more susceptible to M. graminicola infection than wild-type control plants, and conversely, in planta, the silencing of MgGPP through RNAi technology substantially increases the resistance of rice to M. graminicola. Significantly, we show that MgGPP is secreted into host plants and targeted to the ER, where the N-glycosylation and C-terminal proteolysis of MgGPP occur. C-terminal proteolysis promotes MgGPP to leave the ER, after which it is transported to the nucleus. In addition, N-glycosylation of MgGPP is required for suppressing the host response. The research data provide an intriguing example of in planta glycosylation in concert with proteolysis of a pathogen effector, which depict a novel mechanism by which parasitic nematodes could subjugate plant immunity and promote parasitism and may present a promising target for developing new strategies against nematode infections.

A Meloidogyne graminicola C‐type lectin, Mg01965, is secreted into the host apoplast to suppress plant defence and promote parasitism

“…In RKNs, several effector proteins from M. incognita have been shown previously to be delivered into the apoplast of infected tissues by immunocytology, including the calreticulin Mi‐CRT, the amphidial MAP‐1 protein, the aspartyl protease‐like Mi‐ASP2, CBM2‐bearing proteins, pectate lyases and the 6D4 effector (Jaubert et al ., ; Vieira et al ., ). In addition, three RKN effector proteins, Mi‐EFF1 from M. incognita, MJ‐NULG1a from M. javanica and MgGPP from M. graminicola , have been confirmed to be injected into host plants and targeted to giant cell nuclei (Chen et al ., ; Jaouannet et al ., ; Lin et al ., ). Of these effectors, Mi‐CRT and MgGPP have been found to suppress PTI and ETI, respectively (Chen et al ., ; Jaouannet et al ., ).…”

“…In addition, three RKN effector proteins, Mi‐EFF1 from M. incognita, MJ‐NULG1a from M. javanica and MgGPP from M. graminicola , have been confirmed to be injected into host plants and targeted to giant cell nuclei (Chen et al ., ; Jaouannet et al ., ; Lin et al ., ). Of these effectors, Mi‐CRT and MgGPP have been found to suppress PTI and ETI, respectively (Chen et al ., ; Jaouannet et al ., ). Interestingly, more recently, the M. graminicola effector Mg16820 has been found to be secreted in the apoplast during the migration phase of J2s, and in the cytoplasm and the nucleus of giant cells during the early development of the feeding site.…”

“…Sections were incubated in dimethylbenzene and an alcohol gradient to remove paraffin. Subsequently, the sections were immunolocalized using Mg01965 primary antibody and goat anti‐rabbit superclonal secondary antibody, Alexa Fluor 488 conjugate (Thermo Fisher Scientific), sequentially, as described previously (Chen et al ., ). Finally, the sections were mounted with Fluoromount‐G (SouthernBiotech, Birmingham, UK) and observed with a Nikon ECLIPSE Ni microscope (Nikon, Tokyo, Japan).…”

“…More recently, evidence has emerged that M. graminicola secreted effectors can interfere with host immune responses. For instance, the effectors MgGPP and MgMO237 have been shown to suppress plant defences by inhibiting cell death and manipulating rice basal immunity, respectively, thereby promoting M. graminicola parasitism (Chen et al ., ). Although research on M. graminicola effectors is limited, transcriptomic data from different life cycle stages have been reported (Chen et al ., ; Haegeman et al ., ; Petitot et al ., ), offering a starting point to functionally characterize effectors from rice RKNs.…”

The Meloidogyne graminicola effector Mg16820 is secreted in the apoplast and cytoplasm to suppress plant host defense responses

“…Recently, the first effector of M. graminicola , MgGPP, has been functionally analysed by Chen et al . (). This effector targets the endoplasmic reticulum (ER) and, after N ‐glycosylation and C‐terminal proteolysis, the effector is translocated to the nucleus.…”