The role of salicylic acid (SA) and jasmonic acid (JA) signaling in resistance to root pathogens has been poorly documented. We assessed the contribution of SA and JA to basal and partial resistance of Arabidopsis to the biotrophic clubroot agent Plasmodiophora brassicae. SA and JA levels as well as the expression of the SA-responsive genes PR2 and PR5 and the JA-responsive genes ARGAH2 and THI2.1 were monitored in infected roots of the accessions Col-0 (susceptible) and Bur-0 (partially resistant). SA signaling was activated in Bur-0 but not in Col-0. The JA pathway was weakly activated in Bur-0 but was strongly induced in Col-0. The contribution of both pathways to clubroot resistance was then assessed using exogenous phytohormone application and mutants affected in SA or JA signaling. Exogenous SA treatment decreased clubroot symptoms in the two Arabidopsis accessions, whereas JA treatment reduced clubroot symptoms only in Col-0. The cpr5-2 mutant, in which SA responses are constitutively induced, was more resistant to clubroot than the corresponding wild type, and the JA signaling-deficient mutant jar1 was more susceptible. Finally, we showed that the JA-mediated induction of NATA1 drove N(δ)-acetylornithine biosynthesis in infected Col-0 roots. The 35S::NATA1 and nata1 lines displayed reduced or enhanced clubroot symptoms, respectively, thus suggesting that in Col-0 this pathway was involved in the JA-mediated basal clubroot resistance. Overall, our data support the idea that, depending on the Arabidopsis accession, both SA and JA signaling can play a role in partial inhibition of clubroot development in compatible interactions with P. brassicae.

The hypertrophy and hyperplasia of infected roots into clubs are the intrinsic characteristics of clubroot, one of the economically most important diseases in Brassica crops worldwide. Polyamines, arginine (Arg)-derived metabolites, have long been recognized as cell proliferation and differentiation regulators in plants and consequently are suitable candidates for potential gall development factors. Furthermore, Arg catabolism, through arginase, which is strongly connected to polyamine metabolism, would play an important role in response to wound trauma and pathogen infection. In this study, we exploited the Arabidopsis (Arabidopsis thaliana)-Plasmodiophora brassicae pathosystem to investigate the involvement of polyamine metabolism and Arg catabolism in host responses to the pathogen infection and in partial clubroot resistance mechanisms. We demonstrated at the transcriptional, enzymatic, and metabolic levels that polyamine metabolism and Arg catabolism are induced during the later stages of disease in compatible Arabidopsis-P. brassicae interactions. However, susceptible and partially resistant plants showed strikingly different Arg metabolism signatures. Susceptible plants were characterized by a transient agmatine production, a massive induction of arginase, and a strong accumulation of proline. The potential functions of this marked activation of the arginase pathway in the P. brassicae pathogenicity strategy are discussed. Partially resistant plants showed a continuous agmatine production and a weaker arginase pathway activity than the susceptible genotype. Results suggest that the symptom severity was strongly associated to the differential regulation of root polyamine metabolism and Arg catabolism. Further work using arginase transgenic plants will provide insight into the physiological function of the arginase pathway in partial clubroot resistance.Clubroot, caused by the obligate biotrophic protist Plasmodiophora brassicae Woron., is one of the economically most important diseases of Brassica crops in the world. The life cycle of this soil-borne pathogen can be divided into two phases: a primary phase in which events are confined to the root hairs, and a secondary phase that occurs in the cortex and the stele of the hypocotyl and roots of the infected plants. During the second phase, multinucleate plasmodia cause the hypertrophy (abnormal cell enlargement) and hyperplasia (uncontrolled cell division) of infected roots into characteristic clubs (Ingram and Tommerup, 1972). These symptoms obstruct nutrient and water transport, stunt the growth of the plant, and consequently reduce crop yield and quality. Since the pathogen survives as resting spores for a long period (up to 15 years) in the soil, control of the disease by agricultural practices and/or chemical treatments is difficult and/ or expensive. Thus, the development of resistant cultivars is currently the most efficient way to control clubroot among Brassica crops. Both qualitative and quantitative clubroot resistances have been identified and a...

To date, studies of the molecular basis of disease resistance mainly focused on qualitative resistance. However, deciphering mechanisms underlying quantitative resistance could lead to insights into the relationship between qualitative and quantitative resistance and guide the utilization of these two types of resistance to produce durably resistant cultivars. A functional genomics approach, using the CATMA whole-genome microarray, was used to detect changes in gene expression associated with partial quantitative resistance in the Arabidopsis thaliana–Plasmodiophora brassicae pathosystem. The time course of transcript abundance during partial clubroot resistance response was monitored at the whole plant level, and direct comparisons between partial resistance and susceptibility responses were made using the same host genotype. An increasingly complex host response was revealed, as was the differential influence of P. brassicae infection on the transcription of Arabidopsis genes according to the isolate used. We observed, at the transcriptomic level, that metabolic diversion by the pathogen was reduced or delayed, classical plant defense responses were induced earlier and/or more strongly, and cell enlargement and proliferation were actively inhibited in the partial quantitative resistance response compared to the susceptible one.Electronic supplementary materialThe online version of this article (doi:10.1007/s10142-013-0312-9) contains supplementary material, which is available to authorized users.