Date Published: April 12, 2017
Publisher: Public Library of Science
Author(s): Jiansong Chen, Borong Lin, Qiuling Huang, Lili Hu, Kan Zhuo, Jinling Liao, David S. Schneider.
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.
Root-knot nematodes (RKNs) are one of the most economically important plant-parasitic nematodes (PPNs), infecting more than 5500 plant species [1,2]. The soil-borne RKNs devastate varieties of crop plants, resulting in about $70 billion losses in worldwide agriculture annually . Generally, the second-stage juveniles (J2s) of RKNs penetrate host roots and migrate intercellularly towards the vascular cylinder, where they transform five to seven cells around their head into large and multinucleated feeding cells called giant cells that provide RKNs with nutrients and are essential for their development and reproduction . RKNs have evolved numerous effectors that originate from the nematode esophageal gland cells and are secreted into host plant tissues, playing key roles in root invasion and the formation and maintenance of giant cells, resulting in the successful parasitism of RKNs .
In this study, our original aim was to amplify a Meloidogyne avirulence proteins (MAPs) gene based on contigs that were annotated as Map from a previously reported transcriptome of M. graminicola . Although the amplified gene exhibited the highest match with MAPs, the shared identities were no more than 41.1%. Moreover, this gene does not possess a conserved RlpA-like protein domain and internal repetitive motifs, which are common in MAPs [36,37]. These observations showed that the gene is not the counterpart of the reported Map genes of Meloidogyne and is a novel gene that we have called MgGPP.