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

Doron Teper,Jinyun Li,Nian Wang,Jin Xu,Bing Yang

doi:10.1371/journal.ppat.1008886

Doron Teper, Jinyun Li + Show 3 more

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https://doi.org/10.1371/journal.ppat.1008886

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Abstract

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.

Highlights

Xanthomonas are ubiquitous pathogens that cause severe diseases on many crop plants [1]
To examine whether the response of kumquat to Xanthomonas citri subsp. citri (Xcc) harbors hallmarks of immune responses, we investigated the expression of several plant defense-associated genes, Salicylic acid (SA) accumulation, peroxidase activity and production of reactive oxygen species (ROS) at the early and mid-to-late stages of infection
Our study suggests that this durable resistance to Xcc is achieved by multiple mechanisms

Summary

Introduction

Xanthomonas are ubiquitous pathogens that cause severe diseases on many crop plants [1]. Recognition of pathogen elicitors by the plant immune system is mediated through extracellular and intracellular receptor proteins that recognize pathogen-associated molecular patterns (PAMPs), secreted pathogen effectors or plant degradation products [damage-associated molecular patterns (DAMPs)] produced by the activity of hydrolytic enzymes secreted by invading pathogens [2,3,4]. Intracellular immune recognition of translocated pathogen effectors by plant resistance (R) proteins is usually more robust than recognition of PAMPs or DAMPs and in many cases causes localized programmed cell death known as the hypersensitive response (HR) [6]. TALEs are important pathogenicity factors responsible for disease symptoms caused by many Xanthomonas pathogens by activating cognate susceptibility (S) genes. The specific activation occurs by binding to effector binding elements (EBEs) in the promoter regions of S genes through the central repeat region of the TALE [8,9]

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