New Type IV Pili–Related Genes Involved in Early Stages of <i>Ralstonia solanacearum</i> Potato Infection

Siri, María Inés; Sanabria, Analía; Boucher, Christian; Pianzzola, María Julia

doi:10.1094/mpmi-07-13-0210-r

Cited by 21 publications

(17 citation statements)

References 54 publications

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“…Besides their roles in natural transformation and biofilm formation, TFP are also key for bacterial virulence (7). In R. solanacearum, virulence processes during plant colonization have been investigated in some TFP-related genes such as pilA (8) and pilQ (30), highlighting the relationship between twitching motility and virulence (31)(32)(33). Our data demonstrate that PilI and ChpA proteins are required for early pathogenic stages that result in effective plant colonization and wilting.…”

Section: Discussionmentioning

confidence: 79%

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Corral

Sebastià

Coll

et al. 2020

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Ralstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The implication of chemotaxis in plant colonization, through the control flagellar rotation by the proteins CheW and CheA, has been previously reported in R. solanacearum. In this work, we have identified in this bacterium homologues of the Pseudomonas aeruginosa pilI and chpA genes, suggested to play roles in TFP-associated motility analogous to those played by the cheW and cheA genes, respectively. We demonstrate that R. solanacearum strains with a deletion of the pilI or the chpA coding region show normal swimming and chemotaxis but altered biofilm formation and reduced twitching motility, transformation efficiency, and root attachment. Furthermore, these mutants displayed wild-type growth in planta and impaired virulence on tomato plants after soil-drench inoculations but not when directly applied to the xylem. Comparison with deletion mutants for pilA and fliC-encoding the major pilin and flagellin subunits, respectively-showed that both twitching and swimming are required for plant colonization and full virulence. This work proves for the first time the functionality of a pilus-mediated pathway encoded by pil-chp genes in R. solanacearum, demonstrating that pilI and chpA genes are bona fide motility regulators controlling twitching motility and its three related phenotypes: virulence, natural transformation, and biofilm formation. IMPORTANCE Twitching and swimming are two bacterial movements governed by pili and flagella. The present work identifies for the first time in the Gram-negative plant pathogen Ralstonia solanacearum a pilus-mediated chemotaxis pathway analogous to that governing flagellum-mediated chemotaxis. We show that regulatory genes in this pathway control all of the phenotypes related to pili, including twitching motility, natural transformation, and biofilm formation, and are also directly implicated in virulence, mainly during the first steps of the plant infection. Our results show that pili have a higher impact than flagella on the interaction of R. solanacearum with tomato plants and reveal new types of cross-talk between the swimming and twitching motility phenotypes: enhanced swimming in bacteria lacking pili and a role for the flagellum in root attachment.

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Section: Discussionmentioning

confidence: 79%

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Corral

Sebastià

Coll

et al. 2020

mSphere

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“…ripQ and ripS2, two of the three type III secreted effectors inhibited in potato were, respectively, upregulated and not DE in melon, tomato and banana (Ailloud et al, 2016). Interestingly, these two downregulated effectors, together with the also repressed stress response gene speE2 , are located in a genomic region that is deleted in the avirulent R. solanacearum strain UY043 (Siri et al, 2014), which suggests their involvement in bacterial virulence. Similarly, the effector awr5_1 , which was described to trigger hypersensitive response (HR) in tobacco and to inhibit the TOR pathway (Sole et al, 2012; Popa et al, 2016b), showed opposite regulation in potato when compared to tomato and melon (Ailloud et al, 2016), suggesting that it may play host-specific roles.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomes of Ralstonia solanacearum during Root Colonization of Solanum commersonii

et al. 2017

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Bacterial wilt of potatoes—also called brown rot—is a devastating disease caused by the vascular pathogen Ralstonia solanacearum that leads to significant yield loss. As in other plant-pathogen interactions, the first contacts established between the bacterium and the plant largely condition the disease outcome. Here, we studied the transcriptome of R. solanacearum UY031 early after infection in two accessions of the wild potato Solanum commersonii showing contrasting resistance to bacterial wilt. Total RNAs obtained from asymptomatic infected roots were deep sequenced and for 4,609 out of the 4,778 annotated genes in strain UY031 were recovered. Only 2 genes were differentially-expressed between the resistant and the susceptible plant accessions, suggesting that the bacterial component plays a minor role in the establishment of disease. On the contrary, 422 genes were differentially expressed (DE) in planta compared to growth on a synthetic rich medium. Only 73 of these genes had been previously identified as DE in a transcriptome of R. solanacearum extracted from infected tomato xylem vessels. Virulence determinants such as the Type Three Secretion System (T3SS) and its effector proteins, motility structures, and reactive oxygen species (ROS) detoxifying enzymes were induced during infection of S. commersonii. On the contrary, metabolic activities were mostly repressed during early root colonization, with the notable exception of nitrogen metabolism, sulfate reduction and phosphate uptake. Several of the R. solanacearum genes identified as significantly up-regulated during infection had not been previously described as virulence factors. This is the first report describing the R. solanacearum transcriptome directly obtained from infected tissue and also the first to analyze bacterial gene expression in the roots, where plant infection takes place. We also demonstrate that the bacterial transcriptome in planta can be studied when pathogen numbers are low by sequencing transcripts from infected tissue avoiding prokaryotic RNA enrichment.

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“…In fact, c-di-GMP has been found to inhibit motility via several different regulatory mechanisms through controlling transcription, post-transcription, translation, and assembly of flagella stages 32 37 . Additionally, bacterial motility including both flagellar swimming motility and twitching motility mediated by type IV pili (T4P) was also verified to contribute to bacterial virulence 38 . Considering that most flagellar genes in Xoo are located in a single cluster of about 40 ORFs (from XOO2565 to XOO2621), and two other flagellar genes motC (XOO2830) and motB (XOO2831) are located in a chemotaxis cluster downstream of the main flagellar cluster 35 , we therefore further analyzed the expressions of these genes in transcriptional level.…”

Section: Discussionmentioning

confidence: 99%

DgcA, a diguanylate cyclase from Xanthomonas oryzae pv. oryzae regulates bacterial pathogenicity on rice

Xia

Huang

et al. 2016

Sci Rep

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Xanthomonas oryzae pv. oryzae (Xoo) is the causal agent of rice blight disease as well as a serious phytopathogen worldwide. It is also one of the model organisms for studying bacteria-plant interactions. Current progress in bacterial signal transduction pathways has identified cyclic di-GMP as a major second messenger molecule in controlling Xanthomonas pathogenicity. However, it still remains largely unclear how c-di-GMP regulates the secretion of bacterial virulence factors in Xoo. In this study, we focused on the important roles played by DgcA (XOO3988), one of our previously identified diguanylate cyclases in Xoo, through further investigating the phenotypes of several dgcA-related mutants, namely, the dgcA-knockout mutant ΔdgcA, the dgcA overexpression strain OdgcA, the dgcA complemented strain CdgcA and the wild-type strain. The results showed that dgcA negatively affected virulence, EPS production, bacterial autoaggregation and motility, but positively triggered biofilm formation via modulating the intracellular c-di-GMP levels. RNA-seq data further identified 349 differentially expressed genes controlled by DgcA, providing a foundation for a more solid understanding of the signal transduction pathways in Xoo. Collectively, the present study highlights DgcA as a major regulator of Xoo virulence, and can serve as a potential target for preventing rice blight diseases.

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New Type IV Pili–Related Genes Involved in Early Stages of Ralstonia solanacearum Potato Infection

Cited by 21 publications

References 54 publications

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Transcriptomes of Ralstonia solanacearum during Root Colonization of Solanum commersonii

DgcA, a diguanylate cyclase from Xanthomonas oryzae pv. oryzae regulates bacterial pathogenicity on rice

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