Differential Regulation of Root Arginine Catabolism and Polyamine Metabolism in Clubroot-Susceptible and Partially Resistant Arabidopsis Genotypes

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.