Plant Proteins and Processes Targeted by Parasitic Nematode Effectors

Abstract

Sedentary endoparasitic nematodes, such as root-knot nematodes (RKN; Meloidogyne spp.) and cyst nematodes (CN; Heterodera spp. and Globodera spp.) cause considerable damage to agricultural crops. RKN and CN spend most of their life cycle in plant roots, in which they induce the formation of multinucleate hypertrophied feeding cells, called “giant cells” and “syncytia,” respectively. The giant cells result from nuclear divisions of vascular cells without cytokinesis. They are surrounded by small dividing cells and they form a new organ within the root known as a root knot or gall. CN infection leads to the fusion of several root cells into a unique syncytium. These dramatically modified host cells act as metabolic sinks from which the nematode withdraws nutrients throughout its life, and they are thus essential for nematode development. Both RKN and CN secrete effector proteins that are synthesized in the oesophageal glands and delivered to the appropriate cell in the host plant via a syringe-like stylet, triggering the ontogenesis of the feeding structures. Within the plant cell or in the apoplast, effectors associate with specific host proteins, enabling them to hijack important processes for cell morphogenesis and physiology or immunity. Here, we review recent findings on the identification and functional characterization of plant targets of RKN and CN effectors. A better understanding of the molecular determinants of these biotrophic relationships would enable us to improve the yields of crops infected with parasitic nematodes and to expand our comprehension of root development.

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

“…Recent studies showed two PDI-like proteins of PPNs, MgPDI and HsPDI, were localized to the apoplast when GFP fusions were transiently expressed in N. benthamiana (Habash et al, 2017;Tian et al, 2019), indicating their different functional mechanism during nematode parasitism. 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).…”

“…The precise localization of effectors and the identification of their host targets are essential for a better understanding of their biological functions. Only a few host target proteins of RKN effectors have been identified to date (Mejias et al, 2019). The M. incognita effector Mi16D10 has been shown to interact with Arabidopsis SCARECROW-like transcription factors (Huang et al, 2006).…”

The mechanism of potato resistance to Globodera rostochiensis: comparison of root transcriptomes of resistant and susceptible Solanum phureja genotypes

“…The GPCN juveniles penetrate plant roots in which they induce the formation of feeding syncytia. The effector proteins from oesophageal glands trigger the chain of metabolic and morphological changes resulting in fusion of several root cells into a feeding structure as well as suppression of plant immune response [18]. In a few investigations of plant varieties resistant to sedentary nematodes the revealed resistance mechanisms were mainly based on incompatible interaction and hypersensitive response: a zone of dead cells formed either at early or at later stages after infestation isolated juveniles from nutrient supply and prevented completion of their life cycle [19].…”

Surface Sensor Systems in Plant Immunity

“…There are no reports of insect or nematode effectors that directly target PRRs. However, these pests produce numerous effectors which suppress immunity through as yet unknown mechanisms (Hogenhout and Bos, 2011; Mejias et al, 2019), and nematodes are known to manipulate RKs in other signaling pathways through ligand mimicry (Hu and Hewezi, 2018). The identification of additional effectors and their activities is important both to better understand pathogen strategies and to further elucidate the proteins involved in immune signaling and their functions.…”