tepR encoding a bacterial enhancer-binding protein orchestrates the virulence and interspecies competition of Burkholderia glumae through qsmR and a type VI secretion system

Mol Plant Pathol. 2020 Aug;21(8):1042-1054. doi: 10.1111/mpp.12947. Epub 2020 Jul 1.

Abstract

The pathogenesis of the rice pathogenic bacterium Burkholderia glumae is under the tight regulation of the tofI/tofR quorum-sensing (QS) system. tepR, encoding a group I bacterial enhancer-binding protein, negatively regulates the production of toxoflavin, the phytotoxin acting as a major virulence factor in B. glumae. In this study, through a transcriptomic analysis, we identified the genes that were modulated by tepR and/or the tofI/tofR QS system. More than half of the differentially expressed genes, including the genes for the biosynthesis and transport of toxoflavin, were significantly more highly expressed in the ΔtepR mutant but less expressed in the ΔtofI-tofR (tofI/tofR QS-defective) mutant. In consonance with the transcriptome data, other virulence-related functions of B. glumae, extracellular protease activity and flagellum-dependent motility, were also negatively regulated by tepR, and this negative regulatory function of tepR was dependent on the IclR-type transcriptional regulator gene qsmR. Likewise, the ΔtepR mutant exhibited a higher level of heat tolerance in congruence with the higher transcription levels of heat shock protein genes in the mutant. Interestingly, tepR also exhibited its positive regulatory function on a previously uncharacterized type VI secretion system (denoted as BgT6SS-1). The survival of the both ΔtepR and ΔtssD (BgT6SS-1-defective) mutants was significantly compromised compared to the wild-type parent strain 336gr-1 in the presence of the natural rice-inhabiting bacterium, Pantoea sp. RSPAM1. Taken together, this study revealed pivotal regulatory roles of tepR in orchestrating multiple biological functions of B. glumae, including pathogenesis, heat tolerance, and bacterial interspecies competition.

Keywords: burkholderia glumae; qsmR; tepR; bacterial competition; bacterial panicle blight; quorum-sensing; type VI secretion system.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacterial Proteins / metabolism*
  • Burkholderia / metabolism*
  • Burkholderia / pathogenicity*
  • Gene Expression Regulation, Bacterial
  • Quorum Sensing / genetics
  • Quorum Sensing / physiology
  • Type VI Secretion Systems / metabolism*
  • Virulence

Substances

  • Bacterial Proteins
  • Type VI Secretion Systems

Supplementary concepts

  • Burkholderia glumae