Abstract

Plant-parasitic cyst nematodes infect plants and form highly sophisticated feeding sites in roots. It is not known which plant cell signalling mechanisms trigger plant defence during the early stages of nematode parasitism. Mitogen-activated protein kinases (MAPKs) are central components of protein phosphorylation cascades transducing extracellular signals to plant defence responses. MAPK phosphatases control kinase activities and the signalling outcome. The involvement and the role of MPK3 and MPK6, as well as the MAPK phosphatase AP2C1, is demonstrated during parasitism of the beet cyst nematode Heterodera schachtii in Arabidopsis. Our data reveal notable activation patterns of plant MAPKs and the induction of AP2C1 suggesting the attenuation of defence signalling in plant cells during early nematode infection. It is demonstrated that the ap2c1 mutant that is lacking AP2C1 is more attractive but less susceptible to nematodes compared with the AP2C1-overexpressing line. This implies that the function of AP2C1 is a negative regulator of nematode-induced defence. By contrast, the enhanced susceptibility of mpk3 and mpk6 plants indicates a positive role of stress-activated MAPKs in plant immunity against nematodes. Evidence is provided that phosphatase AP2C1, as well as AP2C1-targeted MPK3 and MPK6, are important regulators of plant-nematode interaction, where the co-ordinated action of these signalling components ensures the timely activation of plant defence.

Highlights

  • Sedentary plant-parasitic nematodes, cyst, and root-knot Heterodera schachtii is specialized to exploit Brassicaceae nematodes are the most successful microscopic root endo- and Chenopodiaceae species mainly, including the model parasites (Burrows, 1992)

  • Mitogenactivated protein kinases (MAPKs) activation during different phases of nematode infection, in response to wounding and cellulase treatment In Arabidopsis leaves, MAPKs are rapidly activated by biotic stresses (Asai et al, 2002; Zipfel et al, 2006; SuarezRodriguez et al, 2007; Wu et al, 2007) as well as by mechanical damage (Schweighofer et al, 2007); the activation of MAPK signalling in roots after nematode infection has not been studied so far

  • Our data show a significant increase in nematode development in both mpk3 and mpk6 mutants compared with the wild-type plants (Fig. 6A), suggesting a positive role of both MPK3 and MPK6 in plant defence against the nematodes

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Summary

Introduction

Sedentary plant-parasitic nematodes, cyst, and root-knot Heterodera schachtii is specialized to exploit Brassicaceae nematodes are the most successful microscopic root endo- and Chenopodiaceae species mainly, including the model parasites (Burrows, 1992). Infection process, the nematode second stage juvenile (J2) penetrates the epidermis along the entire root with destructive stylet thrusting and facilitates this by secreting numerous cell wall digesting enzymes that are produced in subventral glands (Wyss, 1992; Goellner et al, 2001). The nematode punctures the cell wall, whereas the plasma membrane remains carefully invaginated. The stylet stays protruded for several hours during which the J2 does not feed. A few hours afterwards, the juvenile starts to withdraw solutes and an increase in cytoplasmic streaming, the proliferation of organelles, alterations in cell wall architecture, and an enlargement of the nuclei (Wyss, 1992) are the first changes in the ISC. The host provides all the nutrients necessary for the completion of the nematode’s life cycle as well as the development and maintenance of the feeding site

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