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Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice.

ABSTRACT: Xanthomonas oryzae pv. oryzae strain PXO99(A) induces the expression of the host gene Os8N3, which results in increased host susceptibility to bacterial blight of rice. Here, we show that PXO99(A) affects the expression of two additional genes in a type III secretion system-dependent manner, one encoding a bZIP transcription factor (OsTFX1) and the other the small subunit of the transcription factor IIA located on chromosome 1 (OsTFIIAgamma1). Induction of OsTFX1 and OsTFIIAgamma1 depended on the type III effector genes pthXo6 and pthXo7, respectively, both encoding two previously undescribed members of the transcription activator-like (TAL) effector family. pthXo7 is strain-specific and may reflect adaptation to the resistance mediated by xa5, an allele of OsTFIIAgamma5 encoding a second form of the TFIIA small subunit on chromosome 5 of rice. The loss of pthXo6 resulted in reduced pathogen virulence, and ectopic expression of OsTFX1 abrogated the requirement for pthXo6 for full virulence. X. oryzae pv. oryzae therefore modulates the expression of multiple host genes using multiple TAL effectors from a single strain, and evidence supports the hypothesis that expression of the associated host genes contributes to host susceptibility to disease.

SUBMITTER: Sugio A

PROVIDER: S-EPMC1965579 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice.

Sugio Akiko A Yang Bing B Zhu Tong T White Frank F FF

Proceedings of the National Academy of Sciences of the United States of America 20070611 25

Xanthomonas oryzae pv. oryzae strain PXO99(A) induces the expression of the host gene Os8N3, which results in increased host susceptibility to bacterial blight of rice. Here, we show that PXO99(A) affects the expression of two additional genes in a type III secretion system-dependent manner, one encoding a bZIP transcription factor (OsTFX1) and the other the small subunit of the transcription factor IIA located on chromosome 1 (OsTFIIAgamma1). Induction of OsTFX1 and OsTFIIAgamma1 depended on th ...[more]

PMID: 17563377

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Project description:Bacterial leaf blight (BLB), caused by Xanthomonas oryzae pv. oryzae (Xoo), gives rise to devastating crop losses in rice. Disease resistant rice cultivars are the most economical way to combat the disease. The TP309 cultivar is susceptible to infection by Xoo strain PXO99. A transgenic variety, TP309_Xa21, expresses the pattern recognition receptor Xa21, and is resistant. PXO99 big up tri, openraxST, a strain lacking the raxST gene, is able to overcome Xa21-mediated immunity. We used a single extraction solvent to demonstrate comprehensive metabolomics and transcriptomics profiling under sample limited conditions, and analyze the molecular responses of two rice lines challenged with either PXO99 or PXO99 big up tri, openraxST. LC-TOF raw data file filtering resulted in better within group reproducibility of replicate samples for statistical analyses. Accurate mass match compound identification with molecular formula generation (MFG) ranking of 355 masses was achieved with the METLIN database. GC-TOF analysis yielded an additional 441 compounds after BinBase database processing, of which 154 were structurally identified by retention index/MS library matching. Multivariate statistics revealed that the susceptible and resistant genotypes possess distinct profiles. Although few mRNA and metabolite differences were detected in PXO99 challenged TP309 compared to mock, many differential changes occurred in the Xa21-mediated response to PXO99 and PXO99 big up tri, openraxST. Acetophenone, xanthophylls, fatty acids, alkaloids, glutathione, carbohydrate and lipid biosynthetic pathways were affected. Significant transcriptional induction of several pathogenesis related genes in Xa21 challenged strains, as well as differential changes to GAD, PAL, ICL1 and Glutathione-S-transferase transcripts indicated limited correlation with metabolite changes under single time point global profiling conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s11306-010-0218-7) contains supplementary material, which is available to authorized users.

Project description:BackgroundXanthomonas oryzae pv. oryzae (Xoo) is the causal agent of rice bacterial blight disease. Xoo produces a range of virulence factors, including EPS, extracellular enzyme, iron-chelating siderophores, and type III-secretion dependent effectors, which are collectively essential for virulence. Genetic and genomics evidence suggest that Xoo might use the diffusible signal factor (DSF) type quorum sensing (QS) system to regulate the virulence factor production. However, little is known about the chemical structure of the DSF-like signal(s) produced by Xoo and the factors influencing the signal production.ResultsXoo genome harbours an rpf cluster comprising rpfB, rpfF, rpfC and rpfG. The proteins encoded by these genes are highly homologous to their counterparts in X. campestris pv. campestris (Xcc), suggesting that Xcc and Xoo might use similar mechanisms for DSF biosynthesis and autoregulation. Consistent with in silico analysis, the rpfF mutant was DSF-deficient and the rpfC mutant produced about 25 times higher DSF-like activity than the wild type Xoo strain KACC10331. From the supernatants of rpfC mutant, we purified three compounds showing strong DSF-like activity. Mass spectrometry and NMR analysis revealed that two of them were the previously characterized DSF and BDSF; the third one was a novel unsaturated fatty acid with 2 double bonds and was designated as CDSF in this study. Further analysis showed that all the three DSF-family signals were synthesized via the enzyme RpfF encoded by Xoo2868. DSF and BDSF at a final concentration of 3 microM to the rpfF mutant could fully restore its extracellular xylanase activity and EPS production to the wild type level, but CDSF was less active than DSF and BDSF in induction of EPS and xylanase. DSF and CDSF shared a similar cell density-dependent production time course with the maximum production being detected at 42 h after inoculation, whereas the maximum production of BDSF was observed at 36 h after inoculation. When grown in a rich medium such as YEB, LB, PSA, and NYG, Xoo produced all the three signals with the majority being DSF. Whereas in nutritionally poor XOLN medium Xoo only produced BDSF and DSF but the majority was BDSF.ConclusionsThis study demonstrates that Xoo and Xcc share the conserved mechanisms for DSF biosynthesis and autoregulation. Xoo produces DSF, BDSF and CDSF signals in rich media and CDSF is a novel signal in DSF-family with two double bonds. All the three DSF-family signals promote EPS production and xylanase activity in Xoo, but CDSF is less active than its analogues DSF and BDSF. The composition and ratio of the three DSF-family signals produced by Xoo are influenced by the composition of culture media.

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Dataset Information

Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice.

Publications

Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice.

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