The soil-borne Gram-negative beta-proteobacterium Ralstonia solanacearum species complex (RSSC) infects more than 250 plant species in over 50 families, causing a devasting bacterial wilt disease that damages crop production worldwide. To develop the control systems for this disease, we need information on the molecular mechanisms underlying the pathogen’s ability to cause disease.
Box 1: Quorum sensing (QS) signalling pathways in Ralstonia pseudosolanacearum strain OE1-1
A phylotype I strain of RSSC, R. pseudosolanacearum strain OE1-1, produces methyl 3-hydroxymyristate (3-OH MAME) as the QS signal, which is synthesised by the methyltransferase PhcB. The 3-OH MAME sensing through the sensor histidine kinase PhcS leads to the phosphorylation of the regulators PhcQ and PhcR; PhcQ and PhcR strongly and partially contribute to the regulation of QS-dependent genes via the LysR family transcription regulator PhcA. The sensor histidine kinase PhcK is required for full expression of phcA, independently of 3-OH MAME sensing. In the active state of QS, PhcA regulates QS-dependent genes responsible for QS-dependent phenotypes including virulence, and induces the production of the virulence-related aryl-furanone secondary metabolites, ralfuranones, and the major exopolysaccharide EPS I. These secondary metabolites are associated with the feedback loop of QS-dependent gene regulation. In the QS active state, expression of lecM encoding the lectin LecM is induced, and LecM affects the stability of extracellularly secreted 3-OH MAME. Furthermore, QS-inducible β-1,4-cellobiohydrolase is involved in not only degradation of plant cell wall degradation but also the full expression of phcA, thereby contributing to the QS feedback loop and virulence of strain OE1-1.
Bacteria monitor “quorum sensing” (QS) signals to track changes in abundance and to activate QS for the synchronous control of the expression of genes beneficial for adaptation to environmental conditions and virulence. In the title image (described fully in Box 1 above), extensive molecular analysis has revealed the complexity of biochemical interactions involved in bacterial colonization of a plant. This box defines what we currently know about R. pseudosolanacearum strain OE1-1 which colonizes growing tomato roots. This bacterium uses QS to regulate colony growth and deployment of plant cell-degrading chemicals inside tomato roots, allowing it to reach the xylem tissue and cause wilt symptoms. The whole understanding of QS signalling pathways may support us to develop counter strategies to control this bacterial wilt disease. However, we do not fully elucidate QS mechanisms here.
This study explores the function of a molecular switch that regulates bacterial quorum sensing. The transcription regulator ChpA receives and regulates molecular signals. (Specifically, it holds a response regulator receiver domain but also a hybrid sensor histidine kinase/response regulator phosphor-acceptor receiver domain and lacks a DNA-binding domain). To explore the function of ChpA in QS of the strain OE1-1, we generated a chpA-deletion mutant (ΔchpA), which exhibited a loss in its infectivity in xylem vessels of tomato plant roots, losing virulence, similarly to the phcA-deletion mutant (ΔphcA). Transcriptome analysis showed that the transcript levels of more than 85% of QS-dependent genes in the ΔchpA were significantly altered compared with the strain OE1-1 and were positively correlated with those in the ΔphcA. Together, ChpA is involved in the regulation of these QS-dependent genes, thereby contributing to the behaviour in host plant roots and virulence of strain OE1-1. These findings will shed light on the full elucidation of QS signalling pathways, allowing us to understand in detail how bacteria exhibit virulence on host plants.
Chika Takemura, Wakana Senuma, Masayuki Tsuzuki, Yuki Terazawa, Kanako Inoue, Masanao Sato, Akinori Kiba, Kouhei Ohnishi, Kenji Kai and Yasufumi Hikichi published this study in Molecular Plant Pathology:
TITLE IMAGE: Proposed model of quorum sensing signalling pathways in Ralstonia pseudosolanacearum strain OE1-1. Image is reproduced from Takemura et al. (2021) and Semuna et al. (2023) with permission of BSPP and John Wiley & Sons. All images used with permission of the author.
