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Rice aquaporin PIP1;3 and harpin Hpa1 of bacterial blight pathogen cooperate in a type III effector translocation.

ABSTRACT: Varieties of Gram-negative bacterial pathogens infect their eukaryotic hosts by deploying the type III translocon to deliver effector proteins into the cytosol of eukaryotic cells in which effectors execute their pathological functions. The translocon is hypothetically assembled by bacterial translocators in association with the assumed receptors situated on eukaryotic plasma membranes. This hypothesis is partially verified in the present study with genetic, biochemical, and pathological evidence for the role of a rice aquaporin, plasma membrane intrinsic protein PIP1;3, in the cytosolic import of the transcription activator-like effector PthXo1 from the bacterial blight pathogen. PIP1;3 interacts with the bacterial translocator Hpa1 at rice plasma membranes to control PthXo1 translocation from cells of a well-characterized strain of the bacterial blight pathogen into the cytosol of cells of a susceptible rice variety. An extracellular loop sequence of PIP1;3 and the α-helix motif of Hpa1 determine both the molecular interaction and its consequences with respect to the effector translocation and the bacterial virulence on the susceptible rice variety. Overall, these results provide multiple experimental avenues to support the hypothesis that interactions between bacterial translocators and their interactors at the target membrane are essential for bacterial effector translocation.

SUBMITTER: Li P

PROVIDER: S-EPMC6598099 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSmall non-coding RNA (sRNA) short sequences regulate various biological processes in all organisms, including bacteria that are animal or plant pathogens. Virulent or pathogenicity-associated sRNAs have been increasingly elucidated in animal pathogens but little is known about similar category of sRNAs in plant-pathogenic bacteria. This is particularly true regarding rice bacterial blight pathogen Xanthomonas oryzae pathovar oryzae (Xoo) as studies on the virulent role of Xoo sRNAs is very limited at present.ResultsThe number and genomic distribution of sRNAs in Xoo were determined by bioinformatics analysis based on high throughput sequencing (sRNA-Seq) of the bacterial cultures from virulence-inducing and standard growth media, respectively. A total of 601 sRNAs were identified in the Xoo genome and ten virulent sRNA candidates were screened out based on significant differences of their expression levels between the culture conditions. In addition, trans3287 and trans3288 were also selected as candidates due to high expression levels in both media. The differential expression of 12 sRNAs evidenced by the sRNA-Seq data was confirmed by a convincing quantitative method. Based on genetic analysis of Xoo ΔsRNA mutants generated by deletion of the 12 single sRNAs, trans217 and trans3287 were characterized as virulent sRNAs. They are essential not only for the formation of bacterial blight in a susceptible rice variety Nipponbare but also for the induction of hypersensitive response (HR) in nonhost plant tobacco. Xoo Δtrans217 and Δtrans3287 mutants fail to induce bacterial blight in Nipponbare and also fail to induce the HR in tobacco, whereas, genetic complementation restores both mutants to the wild type in the virulent performance and HR induction. Similar effects of gene knockout and complementation were found in the expression of hrpG and hrpX genes, which encode regulatory proteins of the type III secretion system. Consistently, secretion of a type III effector, PthXo1, is blocked in Δtrans217 or Δtrans3287 bacterial cultures but retrieved by genetic complementation to both mutants.ConclusionsThe genetic analysis characterizes trans217 and trans3287 as pathogenicity-associated sRNAs essential for the bacterial virulence on the susceptible rice variety and for the HR elicitation in the nonhost plant. The molecular evidence suggests that both virulent sRNAs regulate the bacterial virulence by targeting the type III secretion system.

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Rice aquaporin PIP1;3 and harpin Hpa1 of bacterial blight pathogen cooperate in a type III effector translocation.

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