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.

Keywords: cyst nematodes; effectors; galls; root-knot nematodes; syncytium.

FIGURE 1

Multinucleate and hypertrophied feeding cells induced by endoparasitic plant nematodes. (A) Giant cells (gc and white outline) induced by the root-knot nematode Meloidogyne incognita (rkn and yellow outline) in Arabidopsis thaliana. (B) Syncytium (s and white outline) formed by the cyst nematode Heterodera schachtii in A. thaliana. (A,B) confocal images were obtained by visualizing glutaraldehyde fixative auto-fluorescence after BABB clearing as described in Cabrera et al. (2018). (C) In situ hybridisation of the pioneer M. incognita effector gene Minc16401 encoding a predicted peptide of 69 amino acids (Abad et al., 2008) was performed as described in Jaouannet et al. (2018). Minc16401 expression was localized in subventral glands (svg), suggesting the effector could be secreted in planta via the stylet (st). Bars = 50 μm.