Annals of Botany

Stress responses in plant parasitic nematodes

Well-known as key regulators of cellular signalling in Caenorhabditis elegans and some animal-parasitic nematodes, DAF-16 and SKN-1n transcription factors in the phylum Nematoda modulate many pathways including antioxidant and oxidative stress responses. Gillet et al. provide an overview of the molecular interplay between plant parasitic nematodes (PPN) and their hosts focusing on the early stages of infection.

How do plant-parasitic nematodes alleviate the stress of an apoplast ‘on fire’?
How do plant-parasitic nematodes alleviate the stress of an apoplast ‘on fire’? A model is proposed to explain the DAF-16 and SKN-1 functions that were orchestrated within different cellular pathways to resist the release of toxic compounds (reactive species and phytoalexins) by the plant cell early in infection. In this model, the nematodes sense the physiological state of the plant cell by detecting reactive species, and they generate an adapted response. The findings illustrated in this figure are based primarily on multi-omic resources from plant-parasitic nematodes and functional genomics data from the nematode model system C. elegans. The plant defence response activates the oxidative pathway, leading to the release of reactive species in the apoplast. At the same time, the plant activates its antioxidant pathway to protect the plant cell from oxidative damage. Secondary metabolism is modulated to produce phytoalexins, which represent xenobiotics to the nematode cell. Additionally, the perception of reactive species leads the nematode cell to activate its oxidative stress response. In C. elegans, this pathway is orchestrated by DAF-16 and SKN-1, two transcription factors that are conserved in the animal kingdom. DAF-16 and SKN-1 are negatively regulated by the insulin/IGF-1 signalling (IIS) pathway and positively regulated by miR-71. As in the plant cell, the activation of the antioxidant pathways has a cytoprotective function. In parallel, ROS-scavenging enzymes can be secreted in the apoplast to mitigate the plant’s oxidative burst. The unfolding protein response (UPR) adapts cellular homeostasis and protects proteins directly from oxidative damage induced by oxidative stress. The detoxification pathway covers the phytoalexins produced by the plant cell to suppress their toxicity. GSH, glutathione; CAT, catalase; PER, peroxidase; PRX, peroxiredoxin; SOD, superoxide dismutase; GPX, glutathione peroxidase; SKN-1, skinhead transcription factor-1; DAF-16, dauer formation 16; DAF-12, dauer formation-12; NPR1, non-pathogenic related protein-1; NOX, NADPH oxidase; MTI, MAMP-triggered immunity; MIR-71, micro RNA-71; IIS, insulin IGF1 signalling.

Following initial contact with the host plant roots, plant-parasitic nematodes (PPNs) activate basal immune responses. Defence priming involves the release in the apoplast of toxic molecules derived from reactive species or secondary metabolism. In turn, PPNs must overcome the poisonous and stressful environment at the plant–nematode interface. The ability of PPNs to escape this first line of plant immunity is crucial and will determine its virulence. PPN heterologs of C. elegans DAF-16 and SKN-1 proteins may play a role in successfully bypassing the first line of defence from the host plant. In the context of their hub status and mode of regulation, the authors suggest alternative strategies for control of PPNs through RNAi approaches.

This paper is part of the Annals of Botany Special Issue on Plant Immunity. It will be free access till June 2017 and after April 2018.

Reference

Gillet, F.-X., Bournaud, C., de Souza Júnior, J. D. A., & Fatima Grossi-de-Sa, M. (2017). Plant-parasitic nematodes: towards understanding molecular players in stress responses. Annals of Botany, mcw260. https://doi.org/10.1093/aob/mcw260