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

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.

Experimental evolution of nodule intracellular infection in legume symbionts

“…The R. solanacearum virulence network is orchestrated by the central regulator HrpG that controls a type III secretion machinery (T3SS) and associated effectors via the intermediate regulator HrpB (Poueymiro and Genin, 2009), as well as many genes involved in virulence and host adaptation via a still unknown circuitry (Valls et al, 2006) (Figure 3). hrpG is activated by plant cell contact through the PrhARIJ cascade (Aldon et al, 2000).…”

“…A mutation inactivating vsrA had a weak effect on intracellular infection activation, while two mutations targeting the activation pathway of HrpG (prhI, p 112 hrpG) converted an extracellularly infecting chimeric Ralstonia into a predominantly intracellular legume symbiont. One-hundred and eighty four genes are controlled by HrpG in a HrpBindependent way (Valls et al, 2006), encoding functions such as plant cell-wall degradation, virulence determinants or phytohormone production. Which HrpG-controlled functions negatively impact on intracellular infection remains to be elucidated.…”

Abscisic Acid-Induced Resistance against the Brown Spot Pathogen Cochliobolus miyabeanus in Rice Involves MAP Kinase-Mediated Repression of Ethylene Signaling

“…This ability, together with the production of the JA mimic coronatine and auxins by the same microorganisms, is assumed to contribute to hormonal saturation and consequent circumvention of effectual defenses (Cui et al, 2005;Sreedharan et al, 2006). More recently, Ralstonia solanacearum has been seen to produce ET by means of the HrpG regulon (Valls et al, 2006). Sufficient to affect the plant ET response pathway, bacterial ET production is simultaneous with type 3 secretion system gene expression and contributes to the plant defense imbalance that favors pathogen infection.…”

A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection

“…HrpB expression -and thus that of the T3SS genes -is specifically induced when bacteria are co-cultivated with plant cell suspensions (Marenda et al, 1998), a signal sensed by the outer membrane protein PrhA (Aldon et al, 2000). The activation signal is transferred to hrpB through a regulatory cascade involving the regulators PrhI, PrhJ and HrpG (Brito et al, 2002;Valls et al, 2006). On the other hand, hrpB expression is metabolically repressed during growth in rich medium as compared with minimal medium, which is thought to mimic plant apoplastic fluids (Arlat et al, 1992;Genin et al, 2005).…”