Plants have evolved a series of strategies to combat pathogen infection. Plant SnRK1 is probably involved in shifting carbon and energy use from growth‐associated processes to survival and defence upon pathogen attack, enhancing the resistance to many plant pathogens. The present study demonstrated that SnRK1.1 enhanced the resistance of Arabidopsis thaliana to clubroot disease caused by the plant‐pathogenic protozoan Plasmodiophora brassicae. Through a yeast two‐hybrid assay, glutathione S‐transferase pull‐down assay, and bimolecular fluorescence complementation assay, a P. brassicae RxLR effector, PBZF1, was shown to interact with SnRK1.1. Further expression level analysis of SnRK1.1‐regulated genes showed that PBZF1 inhibited the biological function of SnRK1.1 as indicated by the disequilibration of the expression level of SnRK1.1‐regulated genes in heterogeneous PBZF1‐expressing A. thaliana. Moreover, heterogeneous expression of PBZF1 in A. thaliana promoted plant susceptibility to clubroot disease. In addition, PBZF1 was found to be P. brassicae‐specific and conserved. This gene was significantly highly expressed in resting spores. Taken together, our results provide new insights into how the plant‐pathogenic protist P. brassicae employs an effector to overcome plant resistance, and they offer new insights into the genetic improvement of plant resistance against clubroot disease.

Clubroot caused by Plasmodiophora brassicae is an increasingly important soilborne disease in China. The host range of P. brassicae was investigated with 30 cruciferous plants, including 16 crop species, 9 ornamentals, and 5 weeds in field and pot-cultured conditions. In the field, 17 species from five genera produced visible galls, and these included radish, Capsella bursa-pastoris, Orychophragmus violaceus, Sinapis alba, and 13 Brassica crops. In pot-cultured conditions, an additional 13 plant species (11 genera) were determined to be hosts of P. brassicae. Five common weeds were found to be hosts of P. brassicae, including C. bursa-pastoris, Lepidium apetalum, Descurainia sophia, S. alba, and Thellungiella salsuginea. The infection of these plants was confirmed via polymerase chain reaction (PCR) with primers specific to P. brassicae. No galls were found on Matthiola incana roots in the field or in pots and no resting spores of P. brassicae were observed in M. incana roots, although P. brassicae was detected in M. incana roots via PCR. Microscopic examination revealed infection only in the root hairs of M. incana roots. These results suggested that M. incana was highly resistant to P. brassicae in China and could be developed as a bait crop. In total, 297 accessions of oilseed rape were tested in the field, and 3 accessions of Brassica napus and 1 accession of B. juncea were found to be highly resistant to clubroot disease. These resistant resources provide options for managing clubroot in P. brassicae-infested fields.

Rapeseed (Brassica napus L.) is an important crop for healthy edible oil and stockfeed worldwide. However, its growth and yield are severely hampered by black rot, a destructive disease caused by Xanthomonas campestris pv. campestris (Xcc). Despite the identification of several quantitative trait loci (QTLs) associated with resistance to black rot in Brassica crops, the underlying molecular mechanisms remain largely unexplored. In this study, we investigated Xcc-induced transcriptomic and metabolic changes in the leaves of two rapeseed varieties: Westar (susceptible) and ZS5 (resistant). Our findings indicated that Xcc infection elicited more pronounced overall transcriptomic and metabolic changes in Westar compared to ZS5. Transcriptomic analyses revealed that the phenylpropanoid biosynthesis, cutin, suberine and wax biosynthesis, tryptophan metabolism, and phenylalanine metabolism were enriched in both varieties. Notably, photosynthesis was down-regulated in Westar after infection, whereas this down-regulation occurred at a later stage in ZS5. Integrated analyses of transcriptome and metabolome revealed that the tryptophan metabolism pathway was enriched in both varieties. Indolic glucosinolates and indole-3-acetic acid (IAA) are two metabolites derived from tryptophan. The expression of genes involved in the indolic glucosinolate pathway and the levels of indolic glucosinolates were significantly elevated in both varieties post-infection. Additionally, exogenous application of IAA promoted the development of black rot, whereas the use of an IAA synthesis inhibitor attenuated black rot development in both resistant and susceptible rapeseed varieties. These findings provide valuable molecular insights into the interactions between rapeseed and Xcc, facilitating the advancement of black rot resistance breeding in Brassica crops.