Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells

Abstract

Plant parasitic nematodes are microscopic worms, the most damaging species of which have adopted a sedentary lifestyle within their hosts. These obligate endoparasites have a biotrophic relationship with plants, in which they induce the differentiation of root cells into hypertrophied, multinucleate feeding cells (FCs). Effectors synthesized in the esophageal glands of the nematode are injected into the plant cells via the syringe-like stylet and play a key role in manipulating the host machinery. The establishment of specialized FCs requires these effectors to modulate many aspects of plant cell morphogenesis and physiology, including defense responses. This cell reprogramming requires changes to host nuclear processes. Some proteins encoded by parasitism genes target host nuclei. Several of these proteins were immunolocalized within FC nuclei or shown to interact with host nuclear proteins. Comparative genomics and functional analyses are gradually revealing the roles of nematode effectors. We describe here these effectors and their hypothesized roles in the unique feeding behavior of these pests.

Identification of Plasmodiophora brassicae effectors — A challenging goal

“…Another criterion used to identify putative effectors from obligate intracellular pathogens has been the presence of nuclear localization domains, which allows effectors to directly modulate plant gene expression [58,59]. For many years, effectors capable of migrating to the plant cell nucleus have only been described in bacteria [58–60], but more recently these motifs together with nuclear localization of effectors has been described in fungi [61,62] and nematodes [63]. In bioinformatics pipelines designed to identify putative effectors, the inclusion of steps to remove proteins containing subcellular localization signals will remove these effectors, although researchers could analyze these amino acid sequences directly using the online tool TargetP 1.1 Server (http://www.cbs.dtu.dk/services/TargetP).…”

Not to be suppressed? Rethinking the host response at a root-parasite interface

“…Manipulation of host cell biology by root-knot nematodes to establish infestation sites, including any possible suppression of host defense, is likely to be modulated by effector proteins that are secreted by the nematode during the invasion and induction stages [57]. pathways is much stronger for the cyst nematodes, which are a different sedentary endoparasite that also establish permanent infestation sites in plant roots.…”

“…pathways is much stronger for the cyst nematodes, which are a different sedentary endoparasite that also establish permanent infestation sites in plant roots. Experimentally validated insight into cyst nematode effector proteins is often extrapolated to imply the presence of root-knot nematodes effectors that also interact with the defense pathway [10,57].…”

“…Unlike root-knot nematodes, they also penetrate plant roots in a destructive manner by piercing through plant cells and create their feeding site by inducing the fusion of several plant cells without gall formation on the roots [58]. At present, only one putative effector protein from root-knot nematodes has been tentatively linked to the manipulation of plant defense during infestation [57,59]. Ectopic expression of the root-knot nematode-secreted calreticulin protein was found to suppress the immunity response associated with pathogenic microorganisms when triggered in plant leaves by the bacterial elf18 peptide.…”

Nuclear components and dynamics during plant innate immunity

“…Several articles in this Research Topic highlight these ideas. Quentin et al (2013) describe effectors from plant parasitic nematodes that target host nuclei and possibly interact with nuclear proteins to establish feeding cells in infected plants. In their Original Research article, Ma et al (2013) show that nuclear localization of the Avr2 effector from the xylem-colonizing fungus Fusarium oxysporum is required to trigger I2-mediated resistance in tomato plants, whereas Stam et al (2013) show the diversity of nuclear functions of CRN effectors from the oomycete Phytophthora infestans.…”