Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer reviewed journal
Publication Acceptance Date: 11/13/2007
Publication Date: 3/1/2008
Citation: Wubben, M., Jing, J., Baum, T.J. 2008. Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Molecular Plant-Microbe Interactions. 21:424-432. Interpretive Summary: Salicylic acid is made by plants after pathogen infection so that appropriate defense-related genes can become active. The synthesis of salicylic acid by plants, and the means by which it turns on defense genes, is well studied in the model plant Arabidopsis thaliana. Arabidopsis has been used to investigate the plant defense response to many plant pathogens that infect above-ground plant tissues. However, very little is known about how salicylic acid affects the infection of plants by sedentary plant-parasitic nematodes which only infect plant roots. Plant-parasitic nematodes are major pests of many crops, therefore, any information regarding the discovery of plant defense genes that inhibit their infection may be useful in bioengineering novel plant resistance strategies to nematodes. We analyzed the susceptibility of many Arabidopsis thaliana mutants, which were unable to make salicyclic acid or which were unable to turn on defense genes, to the sugar beet cyst nematode (BCN), Heterodera schachtii. Our work also assessed the expression of multiple plant defense genes in normal and mutant Arabidopsis plants which were infected with BCN. Finally, we measured salicylic acid production in roots of normal Arabidopsis plants infected with BCN. Our data shows that salicylic acid is an important defense compound that inhibits plant infection by cyst nematode. Also, we determined that the expression of some, but not all defense genes, correlates with a plant’s ability to resist cyst nematode infection. Finally, our data suggests that successful cyst nematode infection involves a suppression of salicylic acid production and defense gene expression on the part of the nematode.
Technical Abstract: Compatible interactions between plants and sedentary endoparasitic nematodes, including Heterodera and Meloidogyne spp., require the formation of elaborate feeding sites in proximity to the root vasculature. Feeding site development involves a signal exchange between the host and the nematode and is dependent on the successful evasion of the inducible plant defense response by the parasite. Currently, little is known regarding the identities of plant defense signaling pathways or the genes which comprise them which act to limit nematode parasitism during a compatible interaction. As a step toward resolving this issue, we utilized available Arabidopsis thaliana mutants perturbed in various aspects of salicylic acid (SA)-mediated signaling to investigate the role of this defense compound in inhibiting parasitism by the cyst nematode Heterodera schachtii. We determined that removal of endogenous SA via nahG expression or genetic mutation (sid2, pad4) increased A. thaliana susceptibility to H. schachtii. In contrast, treatment of wild-type plants with SA prior to nematode infection reduced susceptibility. Increased susceptibility to H. schachtii was observed for various npr1 mutant alleles, while the npr1-suppressor mutation sni1 showed decreased susceptibility. Constitutive pathogenesis-related (PR) gene expressing mutants (cpr1, cpr6) did not show altered susceptibility to H. schachtii, however, we determined that constitutive PR gene expression was restricted to shoot tissues in cpr1 plants with wild-type levels of PR-1 transcript present in the roots of this mutant. A time-course experiment revealed that H. schachtii infection elicits an induction of PR-2 and PR-5 in wild-type roots but PR-1 transcript levels remain unaltered. Measurements of total salicylic acid levels within whole wild-type roots infected with H. schachtii showed no accumulation of the compound at 4 days after inoculation. We conclude that salicylic acid acts via NPR1 to inhibit cyst nematode parasitism and that this inhibition is negatively regulated by SNI1. Our results show a strong inverse correlation between basal PR-1 transcript levels and plant susceptibility to H. schachtii and suggest that successful cyst nematode parasitism involves a local suppression of the salicylic acid signaling pathway in infected root tissues.