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.
Highlights
Changes in pathogen gene expression control the switch from a commensal to a parasitic relationship with the host, which may subvert the host metabolism or development to the pathogen’s benefit (Stes et al, 2011)
The Bowtie2 alignment tool with stringent parameters was used, as it retained a number of R. solanacearum reads in mock-inoculated plants that could be considered background levels compared to the high read numbers from inoculated samples (Table 1)
We determined that around 1% of the total sequenced reads from plant tissues corresponded to R. solanacearum and these were retained for further analyses
Summary
Changes in pathogen gene expression control the switch from a commensal to a parasitic relationship with the host, which may subvert the host metabolism or development to the pathogen’s benefit (Stes et al, 2011). There is still limited information concerning how this is controlled. Understanding how these trophic relationships initiate and persist in the host requires deciphering the functional adaptations at the transcriptomic level. Pioneer studies of the expression profiles of bacterial animal pathogens in infected tissues showed that the genes induced more strongly contributed to bacterial virulence and/or survival in the host (reviewed in La et al, 2008). Disease control of bacterial wilt is very challenging, because of the bacterium aggressiveness, its persistence in the field and the lack of resistant commercial varieties in any of its hosts. Potato breeding programs have used wild species related to Solanum tuberosum, such as Solanum commersonii, as sources of resistance against bacterial wilt (Kim-Lee et al, 2005; Siri et al, 2009)
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