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HrpE3 is a type III effector protein required for full virulence of Xanthomonas oryzae pv. oryzicola in rice.

ABSTRACT: Xanthomonas oryzae pv. oryzicola (Xoc) is the causal agent of bacterial leaf streak, a devastating disease in rice. Xoc uses a type III secretion (T3S) system, which is encoded by the hrp-hrc-hpa (hypersensitive response and pathogenicity, hrp-conserved and hrp-associated) genes, to inject repertoires of T3S effectors (T3Es) into plant cells. Many of the hrp-hrc-hpa genes have roles in pathogenesis, but the role of hrpE3, which shows homology to hpaE in X.?campestris pv. vesicatoria (Xcv), is poorly understood. In this study, hrpE3 was shown to be transcribed independent of the hrpD operon, and its expression was dependent on a promoter within hpaB. The expression of hrpE3 was positively regulated by HrpG and HrpX, a finding probably caused by an imperfect plant-inducible promoter (PIP) box (TTCGT-N16 -TTCGA) in the hrpE3 promoter. The secretion of HrpE3 was dependent on T3S, and subcellular localization of HrpE3 was cytoplasmic and nuclear in plant cells. A mutation in hrpE3 reduced the virulence of Xoc by decreasing disease lesion length and bacterial growth in?planta. Full virulence was restored to the mutant when Xoc hrpE3, but not Xcv hpaE, was expressed in?trans. The differences in transcription, secretion via the T3S system and bacterial virulence in plants were attributed to N-terminal amino acid differences between Xoc?HrpE3 and Xcv?HpaE. Collectively, the results demonstrate that hrpE3 encodes a T3E protein which is delivered into the plant cell through the T3S system, localizes to the cytoplasm and nucleus, and is required for full virulence in rice.

SUBMITTER: Cui Y

PROVIDER: S-EPMC6638819 | biostudies-literature | 2013 Sep

REPOSITORIES: biostudies-literature

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HrpE3 is a type III effector protein required for full virulence of Xanthomonas oryzae pv. oryzicola in rice.

Cui Yiping Y Zou Lifang L Zou Huasong H Li Yurong Y Zakria Muhammad M Chen Gongyou G

Molecular plant pathology 20130514 7

Xanthomonas oryzae pv. oryzicola (Xoc) is the causal agent of bacterial leaf streak, a devastating disease in rice. Xoc uses a type III secretion (T3S) system, which is encoded by the hrp-hrc-hpa (hypersensitive response and pathogenicity, hrp-conserved and hrp-associated) genes, to inject repertoires of T3S effectors (T3Es) into plant cells. Many of the hrp-hrc-hpa genes have roles in pathogenesis, but the role of hrpE3, which shows homology to hpaE in X. campestris pv. vesicatoria (Xcv), is po ...[more]

PMID: 23672717

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Project description:Xanthomonas spp. reduce crop yields and quality worldwide. During infection of their plant hosts, many strains secrete transcription activator-like (TAL) effectors, which enter the host cell nucleus and activate specific corresponding host genes at effector binding elements (EBEs) in the promoter. TAL effectors may contribute to disease by activating the expression of susceptibility genes or trigger resistance associated with the hypersensitive reaction (HR) by activating an executor resistance (R) gene. The rice bacterial leaf streak pathogen X. oryzae pv. oryzicola (Xoc) is known to suppress host resistance, and no host R gene has been identified against it, despite considerable effort. To further investigate Xoc suppression of host resistance, we conducted a screen of effectors from BLS256 and identified Tal2a as an HR elicitor in rice when delivered heterologously by a strain of the closely related rice bacterial blight pathogen X. oryzae pv. oryzae (Xoo) or by the soybean pathogen X. axonopodis pv. glycines. The HR required the Tal2a activation domain, suggesting an executor R gene. Tal2a activity was differentially distributed among geographically diverse Xoc isolates, being largely conserved among Asian isolates. We identified four genes induced by Tal2a in next-generation RNA sequencing experiments and confirmed them using quantitative real-time reverse transcription-polymerase chain reaction (qPCR). However, neither individual nor collective activation of these genes by designer TAL effectors resulted in HR. A tal2a knockout mutant of BLS256 showed virulence comparable with the wild-type, but plasmid-based overexpression of tal2a at different levels in the wild-type reduced virulence in a directly corresponding way. Overall, the results reveal that host resistance suppression by Xoc plays a critical role in pathogenesis. Further, the dose-dependent avirulence activity of Tal2a and the apparent lack of a single canonical target that accounts for HR point to a novel, activation domain-dependent mode of action, which might involve, for example, a non-coding gene or a specific pattern of activation across multiple targets.

Project description:The genus Xanthomonas comprises phytopathogenic bacteria which infect about 400 host species, including a wide variety of economically important plants. Xanthomonas oryzae pv. oryzicola (Fang et al., 1957) Swings et al., 1990 is the causal agent of bacterial leaf streak (BLS) being one of the most destructive bacterial diseases of rice. BLS symptoms are very similar to those of bacterial blight caused by closely related Xanthomonas oryzae pv. oryzae. X. o. pv. oryzae and X. o. pv. oryzicola and often occur in rice f ields simultaneously, so separate leaves may show symptoms of both diseases. The quarantine status and high severity of the pathogen require a highly eff icient, fast and precise diagnostic method. We have developed an assay for Xanthomonas oryzae pv. oryzicola detection using real-time polymerase chain reaction (qPCR) and PCR amplicon sequencing. The DNA samples of X. o. pv. oryzae and X. o. pv. oryzicola were obtained from the collection of CIRM-CFBR (France). To evaluate the analytical sensitivity of the assay, a vector construct based on the pAL2-T plasmid was created through the insertion of X. o. pv. oryzicola target fragment (290 bp). Primers and a probe for qPCR were selected for the hpa1 gene site. They allowed identifying all the strains the sequences of which had been loaded in the GenBank NCBI Nucleotide database before November 11, 2021. The SeqX.o.all sequencing primers were selected for the hrp gene cluster sequence, namely for the nucleotide sequence encoding the Hpa1 protein, the sequencing of which allows for eff icient differentiation of X. oryzae species. The analytical specif icity of the system was tested using the DNAs of 53 closely related and accompanying microorganisms and comprised 100 % with no false-positive or false-negative results registered. The system’s analytical sensitivity was not less than 25 copies per PCR reaction. Its eff icacy has been conf irmed using f ive different qPCR detection systems from different manufacturers, so it can be recommended for diagnostic and screening studies.

Dataset Information

HrpE3 is a type III effector protein required for full virulence of Xanthomonas oryzae pv. oryzicola in rice.

Publications

HrpE3 is a type III effector protein required for full virulence of Xanthomonas oryzae pv. oryzicola in rice.

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