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Transcriptomes of Ralstonia solanacearum during Root Colonization of Solanum commersonii.

ABSTRACT: 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.

SUBMITTER: Puigvert M

PROVIDER: S-EPMC5357869 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Transcriptomes of Ralstonia solanacearum during Root Colonization of Solanum commersonii.

Puigvert Marina M Guarischi-Sousa Rodrigo R Zuluaga Paola P Coll Núria S NS Macho Alberto P AP Setubal João C JC Valls Marc M

Frontiers in plant science 20170320

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 resist ...[more]

PMID: 28373879

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Project description:BackgroundSolanum commersonii is a wild potato species that exhibits high tolerance to both biotic and abiotic stresses and has been used as a source of genes for introgression into cultivated potato. Among the interesting features of S. commersonii is resistance to the bacterial wilt caused by Ralstonia solanacearum, one of the most devastating bacterial diseases of crops.ResultsIn this study, we used deep sequencing of S. commersonii RNA (RNA-seq) to analyze the below-ground plant transcriptional responses to R. solanacearum. While a majority of S. commersonii RNA-seq reads could be aligned to the Solanum tuberosum Group Phureja DM reference genome sequence, we identified 2,978 S. commersonii novel transcripts through assembly of unaligned S. commersonii RNA-seq reads. We also used RNA-seq to study gene expression in pathogen-challenged roots of S. commersonii accessions resistant (F118) and susceptible (F97) to the pathogen. Expression profiles obtained from read mapping to the S. tuberosum reference genome and the S. commersonii novel transcripts revealed a differential response to the pathogen in the two accessions, with 221 (F118) and 644 (F97) differentially expressed genes including S. commersonii novel transcripts in the resistant and susceptible genotypes. Interestingly, 22.6% of the F118 and 12.8% of the F97 differentially expressed genes had been previously identified as responsive to biotic stresses and half of those up-regulated in both accessions had been involved in plant pathogen responses. Finally, we compared two different methods to eliminate ribosomal RNA from the plant RNA samples in order to allow dual mapping of RNAseq reads to the host and pathogen genomes and provide insights on the advantages and limitations of each technique.ConclusionsOur work catalogues the S. commersonii transcriptome and strengthens the notion that this species encodes specific genes that are differentially expressed to respond to bacterial wilt. In addition, a high proportion of S. commersonii-specific transcripts were altered by R. solanacearum only in F118 accession, while phythormone-related genes were highly induced in F97, suggesting a markedly different response to the pathogen in the two plant accessions studied.

Project description:Tomato (Solanum lycopersicum L.) is a major Solanaceae crop worldwide and is vulnerable to bacterial wilt (BW) caused by Ralstonia solanacearum during the production process. BW has become a growing concern that could enormously deplete the tomato yield from 50 to 100% and decrease the quality. Research on the molecular mechanism of tomato regulating BW resistance is still limited. In this study, two tomato inbred lines (Hm 2-2, resistant to BW; and BY 1-2, susceptible to BW) were used to explore the molecular mechanism of tomato in response to R. solanacearum infection by RNA-sequencing (RNA-seq) technology. We identified 1923 differentially expressed genes (DEGs) between Hm 2-2 and BY 1-2 after R. solanacearum inoculation. Among these DEGs, 828 were up-regulated while 1095 were down-regulated in R-3dpi (Hm 2-2 at 3 days post-inoculation with R. solanacearum) vs. R-mock (mock-inoculated Hm 2-2); 1087 and 2187 were up- and down-regulated, respectively, in S-3dpi (BY 1-2 at 3 days post-inoculation with R. solanacearum) vs. S-mock (mock-inoculated BY 1-2). Moreover, Gene Ontology (GO) enrichment analysis revealed that the largest amount of DEGs were annotated with the Biological Process terms, followed by Cellular Component and Molecular Function terms. A total of 114, 124, 85, and 89 regulated (or altered) pathways were identified in R-3dpi vs. R-mock, S-3dpi vs. S-mock, R-mock vs. S-mock, and R-3dpi vs. S-3dpi comparisons, respectively, by Kyoto Encyclopaedia of Genes and Genomes (KEGG) pathway analysis. These clarified the molecular function and resistance pathways of DEGs. Furthermore, quantitative RT-PCR (qRT-PCR) analysis confirmed the expression patterns of eight randomly selected DEGs, which suggested that the RNA-seq results were reliable. Subsequently, in order to further verify the reliability of the transcriptome data and the accuracy of qRT-PCR results, WRKY75, one of the eight DEGs was silenced by virus-induced gene silencing (VIGS) and the defense response of plants to R. solanacearum infection was analyzed. In conclusion, the findings of this study provide profound insight into the potential mechanism of tomato in response to R. solanacearum infection, which lays an important foundation for future studies on BW.

Dataset Information

Transcriptomes of Ralstonia solanacearum during Root Colonization of Solanum commersonii.

Publications

Transcriptomes of <i>Ralstonia solanacearum</i> during Root Colonization of <i>Solanum commersonii</i>.

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