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.

Highlights

  • Root-knot nematodes (RKNs) are one of the most economically important plant-parasitic nematodes (PPNs), infecting more than 5500 plant species [1,2]

  • We have shown that the proteolytical processing of MgGPP could change the subcellular trafficking of MgGPP, and the N-glycosylation of MgGPP can activate its function to suppress resistance gene (RBP-1/Gpa2)-mediated cell death, revealing a strategy of host-mediated posttranslational modification (PTM) that is cleverly exploited by plant-parasitic nematodes to subjugate plant immunity and thereby promote parasitism

  • GrUBCEP12 was found to be cleaved in planta [12], suggesting that nematode-secreted effectors may be subjected to posttranslational modification (PTM) in planta

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Summary

Introduction

Root-knot nematodes (RKNs) are one of the most economically important plant-parasitic nematodes (PPNs), infecting more than 5500 plant species [1,2]. Several effectors, mainly cyst nematode-secreted and root-knot nematode-secreted effectors, such as SPRYSEC-19 and GrUBCEP12 in Globodera rostochiensis, Ha-ANNEXIN in Heterodera avenae, MeTCTP in M. enterolobii and MiMsp in M. incognita, were demonstrated to suppress host defense responses directly [9,12,16]. Of these effectors, GrUBCEP12 was found to be cleaved in planta [12], suggesting that nematode-secreted effectors may be subjected to posttranslational modification (PTM) in planta

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