The immunity of Meiwa kumquat against Xanthomonas citri is associated with a known susceptibility gene induced by a transcription activator-like effector.

Citrus canker caused by Xanthomonas citri subsp. citri (Xcc) is one of the most devastating diseases in citrus. Meiwa kumquat (Fortunella crassifolia) has shown a durable resistance against Xcc. Here, we aimed to characterize the mechanisms responsible for such a durable resistance by characterizing the transcriptional and physiological responses of Meiwa kumquat to Xcc. Inoculation of Meiwa kumquat with Xcc promoted immune responses such as upregulation of PR genes, accumulation of salicylic acid, hypersensitive response (HR)-like cell death and early leaf abscission. Hypertrophy and hyperplasia symptoms, which are known to be caused by Xcc-induction of the canker susceptibility gene LOB1 through the transcription activator-like effector (TALE) PthA4, always appear prior to the development of cell death. Mutation of pthA4 in Xcc abolished the induction of LOB1, canker symptoms, cell death, and leaf abscission and reduced the expression of PR genes in inoculated kumquat leaves without reducing Xcc titers in planta. Transcriptome analysis demonstrated that PthA4 promotes plant biotic and abiotic stress responses and the biosynthesis of abscisic acid. Transcriptional induction of LOB1 homologs in Meiwa kumquat by Xcc pthA4 mutant strains carrying a repertoire of designer TALEs promoted the elicitation of HR-like phenotype and leaf abscission, suggesting that kumquat response to Xcc is associated with upregulation of LOB1. Our study suggests a novel mechanism of plant resistance to Xanthomonas via elicitation of immune responses by upregulation of a host susceptibility gene. Author summary: Kumquats, members of the Citrus genus, are known for their durable resistance against citrus canker disease caused by the plant pathogenic bacterium Xanthomonas citri subsp. citri (Xcc). Here, we characterized the resistance mechanisms of Meiwa kumquat to citrus canker. We demonstrate that Xcc infection of Meiwa kumquat causes both immune responses and early leaf abscission, which together contribute to the resistance of kumquat to the pathogen. In addition, we showed that kumquat immune responses and early leaf abscission in the presence of Xcc are elicited by the transcription activator-like effector PthA4, one of the predominant pathogenicity determinants of Xcc in susceptible citrus varieties. PthA4-mediated elicitation of immune responses and early leaf abscission in kumquat occurs via transcriptional induction of the LOB1 gene, which is associated with disease development in susceptible citrus varieties by promoting hypertrophy and hyperplasia symptoms. LOB1 seems to play a dual role in the Xcc-kumquat interaction by acting as a susceptibility gene by promoting hypertrophy and hyperplasia symptoms in the early stages and as a potential activator of immune responses in the late stages; this poses an insurmountable challenge for the pathogen to overcome, contributing to the durable resistance of kumquat to Xcc. [ABSTRACT FROM AUTHOR]