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Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIA?1 to compensate for the absence of OsTFIIA?5 in bacterial blight in rice.

ABSTRACT: Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight (BB) of rice, uses transcription activator-like effectors (TALEs) to interact with the basal transcription factor gamma subunit OsTFIIA?5 (Xa5) and activates the transcription of host genes. However, how OsTFIIA?1, the other OsTFIIA? protein, functions in the presence of TALEs remains unclear. In this study, we show that OsTFIIA?1 plays a compensatory role in the absence of Xa5. The expression of OsTFIIA?1, which is activated by TALE PthXo7, increases the expression of host genes targeted by avirulent and virulent TALEs. Defective OsTFIIA?1 rice lines show reduced expression of the TALE-targeted susceptibility (S) genes, OsSWEET11 and OsSWEET14, which results in increased BB resistance. Selected TALEs (PthXo1, AvrXa7 and AvrXa27) were evaluated for interactions with OsTFIIA?1, Xa5 and xa5 (naturally occurring mutant form of Xa5) using biomolecular fluorescence complementation (BiFC) and microscale thermophoresis (MST). BiFC and MST demonstrated that the three TALEs bind Xa5 and OsTFIIA?1 with a stronger affinity than xa5. These results provide insights into the complex roles of OsTFIIA?1 and OsTFIIA?5 in TALE-mediated host gene transcription.

SUBMITTER: Ma W

PROVIDER: S-EPMC6638009 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIAγ1 to compensate for the absence of OsTFIIAγ5 in bacterial blight in rice.

Ma Wenxiu W Zou Lifang L Zhiyuan J I JI Xiameng X U XU Zhengyin X U XU Yang Yangyang Y Alfano James R JR Chen Gongyou G

Molecular plant pathology 20180807 10

Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight (BB) of rice, uses transcription activator-like effectors (TALEs) to interact with the basal transcription factor gamma subunit OsTFIIAγ5 (Xa5) and activates the transcription of host genes. However, how OsTFIIAγ1, the other OsTFIIAγ protein, functions in the presence of TALEs remains unclear. In this study, we show that OsTFIIAγ1 plays a compensatory role in the absence of Xa5. The expression of OsTFIIAγ1, which is activa ...[more]

PMID: 29704467

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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.

Project description:TITLE: Transcriptional profiling of Rgene-mediated responses in rice PROJECT DESCRIPTION: The dominant gene Xa7 and the recessive gene xa5 of rice confer resistance to several races of the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Xoo). To reveal the modes of action and the defense responses these genes initiate, we decided to obtain the global transcriptional profiles of the rice cultivars IRBB7, IRBB5 (which harbor Xa7 and xa5, respectively) and IR24 undergoing early infection by the Xoo Race 2 strain PXO86. Both IRBB7 and IRBB5 are resistant to PXO86 (which carry the corresponding avirulence genes avrXa7 and avrxa5), whereas IR24 is susceptible. We inoculated by vacuum infiltration the three rice cultivars ten days after seed germination (or 2 weeks after sowing) and collected inoculated tissue at 5 different timepoints within the first day after inoculation. The transcriptional profiles obtained will provide valuable insight into the similarities and differences between incompatible interactions mediated by a dominant and a recessive Rgene, in comparison to a compatible interaction. ****[PLEXdb(http://www.plexdb.org) has submitted this series at GEO on behalf of the original contributor, David O Nino-Liu. The equivalent experiment is OS4 at PLEXdb.] genotype: IR24 - time: 0 hai(3-replications); genotype: IR24 - time: 3 hai(3-replications); genotype: IR24 - time: 6 hai(3-replications); genotype: IR24 - time: 12 hai(3-replications); genotype: IR24 - time: 24 hai(3-replications); genotype: IRBB5 - time: 0 hai(3-replications); genotype: IRBB5 - time: 3 hai(3-replications); genotype: IRBB5 - time: 6 hai(3-replications); genotype: IRBB5 - time: 12 hai(3-replications); genotype: IRBB5 - time: 24 hai(3-replications); genotype: IRBB7 - time: 0 hai(3-replications); genotype: IRBB7 - time: 3 hai(3-replications); genotype: IRBB7 - time: 6 hai(3-replications); genotype: IRBB7 - time: 12 hai(3-replications); genotype: IRBB7 - time: 24 hai(3-replications)

Project description:Most Xanthomonas species translocate Transcription Activator-Like (TAL) effectors into plant cells where they function like plant transcription factors via a programmable DNA-binding domain. Characterized strains of rice pathogenic X. oryzae pv. oryzae harbor 9-16 different tal effector genes, but the function of only a few of them has been decoded. Using sequencing of entire genomes, we first performed comparative analyses of the complete repertoires of TAL effectors, herein referred to as TALomes, in three Xoo strains forming an African genetic lineage different from Asian Xoo. A phylogenetic analysis of the three TALomes combined with in silico predictions of TAL effector targets showed that African Xoo TALomes are highly conserved, genetically distant from Asian ones, and closely related to TAL effectors from the bacterial leaf streak pathogen Xanthomonas oryzae pv. oryzicola (Xoc). Nine clusters of TAL effectors could be identified among the three TALomes, including three showing higher levels of variation in their repeat variable diresidues (RVDs). Detailed analyses of these groups revealed recombination events as a possible source of variation among TAL effector genes. Next, to address contribution to virulence, nine TAL effector genes from the Malian Xoo strain MAI1 and four allelic variants from the Burkinabe Xoo strain BAI3, thus representing most of the TAL effector diversity in African Xoo strains, were expressed in the TAL effector-deficient X. oryzae strain X11-5A for gain-of-function assays. Inoculation of the susceptible rice variety Azucena lead to the discovery of three TAL effectors promoting virulence, including two TAL effectors previously reported to target the susceptibility (S) gene OsSWEET14 and a novel major virulence contributor, TalB. RNA profiling experiments in rice and in silico prediction of EBEs were carried out to identify candidate targets of TalB, revealing OsTFX1, a bZIP transcription factor previously identified as a bacterial blight S gene, and OsERF#123, which encodes a subgroup IXc AP2/ERF transcription factor. Use of designer TAL effectors demonstrated that induction of either gene resulted in greater susceptibility to strain X11-5A. The induction of OsERF#123 by BAI3Δ1, a talB knockout derivative of BAI3, carrying these designer TAL effectors increased virulence of BAI3Δ1, validating OsERF#123 as a new, bacterial blight S gene.

Dataset Information

Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIA?1 to compensate for the absence of OsTFIIA?5 in bacterial blight in rice.

Publications

Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIAγ1 to compensate for the absence of OsTFIIAγ5 in bacterial blight in rice.

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