Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots.

Compatible plant-nematode interactions involve the formation of an elaborate feeding site within the host root that requires the evasion of plant defense mechanisms by the parasite. Little is known regarding plant defense signaling pathways that limit nematode parasitism during a compatible interaction. Therefore, we utilized Arabidopsis thaliana mutants perturbed in salicylic acid (SA) biosynthesis or signal transduction to investigate the role of SA in inhibiting parasitism by the beet cyst nematode Heterodera schachtii. We determined that SA-deficient mutants (sid2-1, pad4-1, and NahG) exhibited increased susceptibility to H. schachtii. In contrast, SA-treated wild-type plants showed decreased H. schachtii susceptibility. The npr1-2 and npr1-3 mutants, which are impaired in SA signaling, also showed increased susceptibility to H. schachtii, whereas the npr1-suppressor mutation sni1 showed decreased susceptibility. Constitutive pathogenesis-related (PR) gene-expressing mutants (cpr1 and cpr6) did not show altered susceptibility to H. schachtii; however, constitutive PR gene expression was restricted to cpr1 shoots with wild-type levels of PR-1 transcript present in cpr1 roots. Furthermore, we determined that H. schachtii infection elicits SA-independent PR-2 and PR-5 induction in wild-type roots, while PR-1 transcript and total SA levels remained unaltered. This was in contrast to shoots of infected plants where PR-1 transcript abundance and total SA levels were elevated. We conclude that SA acts via NPR1 to inhibit nematode parasitism which, in turn, is negatively regulated by SNI1. Our results show an inverse correlation between root basal PR-1 expression and plant susceptibility to H. schachtii and suggest that successful cyst nematode parasitism may involve a local suppression of SA signaling in roots.

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