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Abstract

The plant hormone salicylic acid (SA) plays a critical role in defense against biothrophic pathogens such as Plasmodiophora brassicae (Pb) which is an obligate pathogen of crucifer species and the causal agent of clubroot disease of canola (Brassica napus). Pb encodes a protein, predicted to be secreted, with very limited homology to benzoic acid (BA)/SA –methyltransferase (MT) designated PbBSMT. PbBSMT has a SA- and an IAA-binding domain, which are also present in Arabidopsis thaliana BSMT1 (AtBSMT1), and these domains in PbBSMT methylate BA and SA. In support of the hypothesis that Pb uses PbBSMT to overcome SA-mediated defenses by converting SA into inactive methyl salicylate (MeSA), here we show that PbBSMT suppresses local defense and provide evidence that PbBSMT is much more effective than AtBSMT1 at suppressing the levels of SA and its associated effects. Basal SA levels in Arabidopsis plants that constitutively overexpressing PbBSMT compared to those in Arabidopsis wild type Col-0 (WT) were reduced approximately 80% verses only a 50% reduction in plants overexpressing AtBSMT1. PbBSMT-overexpressing plants were more susceptible to Pb than WT plants; they also were partially compromised in non-host resistance to Albugo candida. In contrast, AtBSMT1 response to either Pb or A. candida was similar to the control WT Col. Furthermore, transgenic Arabidopsis and tobacco plants overexpressing PbBSMT exhibited increase susceptibility to virulent Pseudomonas syringae pv. tomato DC3000 and virulent P. syringae pv. tabaci, respectively. R-gene mediated resistance to PstDC3000/AvrRpt2 and TMV was also compromised in Arabidopsis and Nicotiana tabacum cv. Xanthi-nc plants overexpressing PbBSMT, respectively. Transient expression of PbBSMT or AtBSMT1 in lower leaves of Nt Xanthi-nc resulted in systemic acquired resistance (SAR)-like enhanced resistance to TMV in the distal systemic leaves. Chimeric grafting experiments revealed that similar to SAR, the development of PbBSMT-mediated SAR-like phenotype was also dependent on the MeSA esterase activity of NtSABP2 in the systemic leaves. Collectively, these results strongly suggest that PbBSMT is a novel effector, which is secreted by Pb into its host plant to deplete pathogen-induced SA accumulation.