Hydathode immunity against the vascular pathogenXanthomonas campestrispv. campestris by the Arabidopsis CNL-type receptor SUT1

Abstract

AbstractBacterial plant pathogens exploit natural openings, such as pores or wounds, to enter the plant interior and cause disease. Plants actively guard these openings through defense mechanisms that have been described extensively for stomates, the most common points of entry. However, bacteria from the genusXanthomonashave specialized in that they enter their host via hydathodes—a poorly studied organ at the leaf margin involved in guttation. While hydathodes can mount an effective immune response against bacteria, a dedicated perception mechanism still needs to be discovered. To identify a hydathode-specific immune receptor, we mapped a novel resistance gene againstX. campestrispv. campestris (Xcc) in Arabidopsis using an inoculation procedure that promotes natural entry via hydathodes. Using Recombinant Inbred Lines (RILs) between susceptible accession Oy-0 and resistant Col-0, a QTL for resistance was identified on the right arm of Chromosome 5 in Col-0. Combining this finding with results of a genome-wide association analysis, a single candidate gene was fine-mapped that encoded a coiled-coil nucleotide-binding leucine-rich repeat (CNL) immune receptor protein called SUPPRESSOR OF TOPP4 1 (SUT1). Whereas the ZAR1 immune receptor acts in the vasculature against Xcc, we establish that SUT1 already restricts Xcc in hydathodes but is ineffective in the vasculature. In corroboration, we confirm promoter activity ofSUT1in the epithem tissue within hydathodes. Altogether, we provide evidence for an NLR that confers hydathode-specific resistance in Arabidopsis against infection by Xcc.Author summaryBlack rot disease, caused by the bacterial pathogenXanthomonas campestrispv. campestris (Xcc), is an economically relevant disease of cabbage crops. Xcc is rather unique in that it enters the plant interior through specialized organs at the edge of the leaf. These structures called hydathodes contain water pores and are involved in leaf water regulation. Although we know that hydathodes can mount an immune response against these bacteria, specific immune receptors still need to be discovered. In our search for hydathode resistance mechanisms, we use the model plantArabidopsis thalianato identify genetic targets that could be translated to cabbage breeding practices. Here, by screening large populations of genetically diverse Arabidopsis plants, we could pinpoint a genetic locus that is involved in hydathode resistance. On this locus, we identified a gene,SUT1, that confers resistance against Xcc, restricting early hydathode colonization by the bacteria and reducing subsequent disease symptoms. Interestingly, this resistance is ineffective in later stages of infection when the bacteria colonize the plant vascular system. Therefore, this study provides new insights in hydathode-specific resistance and opens doors for more research on these tissue- or organ-specific resistance mechanisms in plants.