The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato
ABSTRACT Plant xylem fluid is considered a nutrient-poor environment, but the bacterial wilt pathogen Ralstonia solanacearum is well adapted to it, growing to 108 to 109 CFU/g tomato stem. To better understand how R. solanacearum succeeds in this habitat, we analyzed the transcriptomes of two phylog...
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American Society for Microbiology
2012
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oai:doaj.org-article:13f54c2367d8461995df02596cbc81952021-11-15T15:39:09ZThe <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato10.1128/mBio.00114-122150-7511https://doaj.org/article/13f54c2367d8461995df02596cbc81952012-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00114-12https://doaj.org/toc/2150-7511ABSTRACT Plant xylem fluid is considered a nutrient-poor environment, but the bacterial wilt pathogen Ralstonia solanacearum is well adapted to it, growing to 108 to 109 CFU/g tomato stem. To better understand how R. solanacearum succeeds in this habitat, we analyzed the transcriptomes of two phylogenetically distinct R. solanacearum strains that both wilt tomato, strains UW551 (phylotype II) and GMI1000 (phylotype I). We profiled bacterial gene expression at ~6 × 108 CFU/ml in culture or in plant xylem during early tomato bacterial wilt pathogenesis. Despite phylogenetic differences, these two strains expressed their 3,477 common orthologous genes in generally similar patterns, with about 12% of their transcriptomes significantly altered in planta versus in rich medium. Several primary metabolic pathways were highly expressed during pathogenesis. These pathways included sucrose uptake and catabolism, and components of these pathways were encoded by genes in the scrABY cluster. A UW551 scrA mutant was significantly reduced in virulence on resistant and susceptible tomato as well as on potato and the epidemiologically important weed host Solanum dulcamara. Functional scrA contributed to pathogen competitive fitness during colonization of tomato xylem, which contained ~300 µM sucrose. scrA expression was induced by sucrose, but to a much greater degree by growth in planta. Unexpectedly, 45% of the genes directly regulated by HrpB, the transcriptional activator of the type 3 secretion system (T3SS), were upregulated in planta at high cell densities. This result modifies a regulatory model based on bacterial behavior in culture, where this key virulence factor is repressed at high cell densities. The active transcription of these genes in wilting plants suggests that T3SS has a biological role throughout the disease cycle. IMPORTANCE Ralstonia solanacearum is a widespread plant pathogen that causes bacterial wilt disease. It inflicts serious crop losses on tropical farmers, with major economic and human consequences. It is also a model for the many destructive microbes that colonize the water-conducting plant xylem tissue, which is low in nutrients and oxygen. We extracted bacteria from infected tomato plants and globally identified the biological functions that R. solanacearum expresses during plant pathogenesis. This revealed the unexpected presence of sucrose in tomato xylem fluid and the pathogen’s dependence on host sucrose for virulence on tomato, potato, and the common weed bittersweet nightshade. Further, R. solanacearum was highly responsive to the plant environment, expressing several metabolic and virulence functions quite differently in the plant than in pure culture. These results reinforce the utility of studying pathogens in interaction with hosts and suggest that selecting for reduced sucrose levels could generate wilt-resistant crops.Jonathan M. JacobsLavanya BabujeeFanhong MengAnnett MillingCaitilyn AllenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 4 (2012) |
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Microbiology QR1-502 |
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Microbiology QR1-502 Jonathan M. Jacobs Lavanya Babujee Fanhong Meng Annett Milling Caitilyn Allen The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| description |
ABSTRACT Plant xylem fluid is considered a nutrient-poor environment, but the bacterial wilt pathogen Ralstonia solanacearum is well adapted to it, growing to 108 to 109 CFU/g tomato stem. To better understand how R. solanacearum succeeds in this habitat, we analyzed the transcriptomes of two phylogenetically distinct R. solanacearum strains that both wilt tomato, strains UW551 (phylotype II) and GMI1000 (phylotype I). We profiled bacterial gene expression at ~6 × 108 CFU/ml in culture or in plant xylem during early tomato bacterial wilt pathogenesis. Despite phylogenetic differences, these two strains expressed their 3,477 common orthologous genes in generally similar patterns, with about 12% of their transcriptomes significantly altered in planta versus in rich medium. Several primary metabolic pathways were highly expressed during pathogenesis. These pathways included sucrose uptake and catabolism, and components of these pathways were encoded by genes in the scrABY cluster. A UW551 scrA mutant was significantly reduced in virulence on resistant and susceptible tomato as well as on potato and the epidemiologically important weed host Solanum dulcamara. Functional scrA contributed to pathogen competitive fitness during colonization of tomato xylem, which contained ~300 µM sucrose. scrA expression was induced by sucrose, but to a much greater degree by growth in planta. Unexpectedly, 45% of the genes directly regulated by HrpB, the transcriptional activator of the type 3 secretion system (T3SS), were upregulated in planta at high cell densities. This result modifies a regulatory model based on bacterial behavior in culture, where this key virulence factor is repressed at high cell densities. The active transcription of these genes in wilting plants suggests that T3SS has a biological role throughout the disease cycle. IMPORTANCE Ralstonia solanacearum is a widespread plant pathogen that causes bacterial wilt disease. It inflicts serious crop losses on tropical farmers, with major economic and human consequences. It is also a model for the many destructive microbes that colonize the water-conducting plant xylem tissue, which is low in nutrients and oxygen. We extracted bacteria from infected tomato plants and globally identified the biological functions that R. solanacearum expresses during plant pathogenesis. This revealed the unexpected presence of sucrose in tomato xylem fluid and the pathogen’s dependence on host sucrose for virulence on tomato, potato, and the common weed bittersweet nightshade. Further, R. solanacearum was highly responsive to the plant environment, expressing several metabolic and virulence functions quite differently in the plant than in pure culture. These results reinforce the utility of studying pathogens in interaction with hosts and suggest that selecting for reduced sucrose levels could generate wilt-resistant crops. |
| format |
article |
| author |
Jonathan M. Jacobs Lavanya Babujee Fanhong Meng Annett Milling Caitilyn Allen |
| author_facet |
Jonathan M. Jacobs Lavanya Babujee Fanhong Meng Annett Milling Caitilyn Allen |
| author_sort |
Jonathan M. Jacobs |
| title |
The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| title_short |
The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| title_full |
The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| title_fullStr |
The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| title_full_unstemmed |
The <italic toggle="yes">In Planta</italic> Transcriptome of <named-content content-type="genus-species">Ralstonia solanacearum</named-content>: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato |
| title_sort |
<italic toggle="yes">in planta</italic> transcriptome of <named-content content-type="genus-species">ralstonia solanacearum</named-content>: conserved physiological and virulence strategies during bacterial wilt of tomato |
| publisher |
American Society for Microbiology |
| publishDate |
2012 |
| url |
https://doaj.org/article/13f54c2367d8461995df02596cbc8195 |
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