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

Abstract

On invasion of roots, plant-parasitic nematodes secrete effectors to manipulate the cellular regulation of the host to promote parasitism. The root-knot nematode Meloidogyne graminicola is one of the most damaging nematodes of rice. Here, we identified a novel effector of this nematode, named Mg16820, expressed in the nematode subventral glands. We localized the Mg16820 effector in the apoplast during the migration phase of the second-stage juvenile in rice roots. In addition, during early development of the feeding site, Mg16820 was localized in giant cells, where it accumulated in the cytoplasm and the nucleus. Using transient expression in Nicotiana benthamiana leaves, we demonstrated that Mg16820 directed to the apoplast was able to suppress flg22-induced reactive oxygen species production. In addition, expression of Mg16820 in the cytoplasm resulted in the suppression of the R2/Avr2- and Mi-1.2-induced hypersensitive response. A potential target protein of Mg16820 identified with the yeast two-hybrid system was the dehydration stress-inducible protein 1 (DIP1). Bimolecular fluorescence complementation resulted in a strong signal in the nucleus. DIP1 has been described as an abscisic acid (ABA)-responsive gene and ABA is involved in the biotic and abiotic stress response. Our results demonstrate that Mg16820 is able to act in two cellular compartments as an immune suppressor and targets a protein involved in the stress response, therefore indicating an important role for this effector in parasitism.

The root‐knot nematode effector MiPDI1 targets a stress‐associated protein (SAP) to establish disease in Solanaceae and Arabidopsis

“…Despite the hundreds of effectors characterized (Mejias et al, 2019), few RKN effectors have been demonstrated to be secreted in planta and to target giant cells. Example of effectors are the M. incognita Mi-EFF1 (Jaouannet et al, 2012) and MiMIF-2 (Zhao et al, 2019), the Meloidogyne javanica MjNULG1a (Lin et al, 2016) and the M. graminicola MgGPP (Chen et al, 2017) and Mg16820 (Naalden et al, 2018). We also showed that the silencing of MiPDI1 in planta affected the number of galls and egg masses obtained and delayed nematode development.…”

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

“…When Mg16820 localizes in the apoplast, it can suppress PTI. However, Mg16820 directed to the cytoplasm is able to suppress ETI (Naalden et al, 2018a). All of these results suggest that RKN-secreted effectors can suppress plant defence responses within different plant cell compartment(s), probably using different mechanisms.…”

Plant defense responses in monocotyledonous and dicotyledonous host plants during root-knot nematode infection

“…Moreover, the effector protein MjTTL5 from M. javanica promotes plant ROSscavenging activity and suppresses host defenses (Lin et al 2016). For another effector protein, Mg16820, encoded by M. graminicola and localized in the apoplast, cytoplasm and nucleus of plant cells, the potential target protein in plants is dehydration-stress inducible protein 1 (DIP1), which was reported as an ABA-responsive gene (Naalden et al 2018). Mg16820 functions in the apoplast and in the cytoplasm by interacting with components important in ROS defense signaling, which may suggest that this protein is able to interfere with two different mechanisms to suppress the immune system of the plant.…”