Integrated Regulation of the Type III Secretion System and Other Virulence Determinants in Ralstonia solanacearum

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Abstract
In many plant and animal bacterial pathogens, the Type III secretion system (TTSS) that directly translocates effector proteins into the eukaryotic host cells is essential for the development of disease. In all species studied, the transcription of the TTSS and most of its effector substrates is tightly regulated by a succession of consecutively activated regulators. However, the whole genetic programme driven by these regulatory cascades is still unknown, especially in bacterial plant pathogens. Here, we have characterised the programme triggered by HrpG, a host-responsive regulator of the TTSS activation cascade in the plant pathogen Ralstonia solanacearum. We show through genome-wide expression analysis that, in addition to the TTSS, HrpG controls the expression of a previously undescribed TTSS-independent pathway that includes a number of other virulence determinants and genes likely involved in adaptation to life in the host. Functional studies revealed that this second pathway co-ordinates the bacterial production of plant cell wall-degrading enzymes, exopolysaccharide, and the phytohormones ethylene and auxin. We provide experimental evidence that these activities contribute to pathogenicity. We also show that the ethylene produced by R. solanacearum is able to modulate the expression of host genes and can therefore interfere with the signalling of plant defence responses. These results provide a new, integrated view of plant bacterial pathogenicity, where a common regulator activates synchronously upon infection the TTSS, other virulence determinants and a number of adaptive functions, which act co-operatively to cause disease. Most pathogenic bacteria have the ability to switch between free-living growth and life within the host tissues. However, the mechanisms that co-ordinate changes in gene expression during the passage between these alternative ecological niches are still largely unknown. A well-studied regulation pathway triggered in response to the host environment is that controlling the transcription of the Type III secretion system (TTSS) genes. The TTSS is a major pathogenicity determinant that delivers bacterial effector proteins directly into the host cell cytosol to promote disease. Here, Valls and colleagues show that the TTSS regulatory pathway is directly connected with other circuits driving the expression of diverse pathogenicity and host-adaptation activities. The authors have identified and characterised the genes co-regulated along with the TTSS via the HrpG regulator. They have found that, in addition to the TTSS, HrpG controls the transcription of a previously unknown TTSS-independent pathway that is essential to pathogenicity and alters the bacterial production of plant cell wall-degrading enzymes, exopolysaccharide, and the phytohormones ethylene and auxin. These findings reveal an important degree of co-ordination between adaptation and virulence functions at the transcriptional level and contribute to a better understanding of the infection process.