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Transcriptome Analysis Reveals New Insights into the Bacterial Wilt Resistance Mechanism Mediated by Silicon in Tomato.

ABSTRACT: Bacterial wilt is a devastating disease of tomato caused by soilborne pathogenic bacterium Ralstonia solanacearum. Previous studies found that silicon (Si) can increase tomato resistance against R. solanacearum, but the exact molecular mechanism remains unclear. RNA sequencing (RNA-Seq) technology was used to investigate the dynamic changes of root transcriptome profiles between Si-treated (+Si) and untreated (-Si) tomato plants at 1, 3, and 7 days post-inoculation with R. solanacearum. The contents of salicylic acid (SA), ethylene (ET), and jasmonic acid (JA) and the activity of defense-related enzymes in roots of tomato in different treatments were also determined. The burst of ET production in roots was delayed, and SA and JA contents were altered in Si treatment. The transcriptional response to R. solanacearum infection of the +Si plants was quicker than that of the untreated plants. The expression levels of differentially-expressed genes involved in pathogen-associated molecular pattern-triggered immunity (PTI), oxidation resistance, and water-deficit stress tolerance were upregulated in the Si-treated plants. Multiple hormone-related genes were differentially expressed in the Si-treated plants. Si-mediated resistance involves mechanisms other than SA- and JA/ET-mediated stress responses. We propose that Si-mediated tomato resistance to R. solanacearum is associated with activated PTI-related responses and enhanced disease resistance and tolerance via several signaling pathways. Such pathways are mediated by multiple hormones (e.g., SA, JA, ET, and auxin), leading to diminished adverse effects (e.g., senescence, water-deficit, salinity and oxidative stress) normally caused by R. solanacearum infection. This finding will provide an important basis to further characterize the role of Si in enhancing plant resistance against biotic stress.

SUBMITTER: Jiang N

PROVIDER: S-EPMC6387441 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Transcriptome Analysis Reveals New Insights into the Bacterial Wilt Resistance Mechanism Mediated by Silicon in Tomato.

Jiang Nihao N Fan Xueying X Lin Weipeng W Wang Guoping G Cai Kunzheng K

International journal of molecular sciences 20190211 3

Bacterial wilt is a devastating disease of tomato caused by soilborne pathogenic bacterium Ralstonia solanacearum. Previous studies found that silicon (Si) can increase tomato resistance against R. solanacearum, but the exact molecular mechanism remains unclear. RNA sequencing (RNA-Seq) technology was used to investigate the dynamic changes of root transcriptome profiles between Si-treated (+Si) and untreated (-Si) tomato plants at 1, 3, and 7 days post-inoculation with R. solan ...[more]

PMID: 30754671

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Project description:Ralstonia solanacearum causes bacterial wilt disease, leading to severe crop losses. Xylem sap from R. solanacearum-infected tomato is enriched in the disaccharide trehalose. Water-stressed plants also accumulate trehalose, which increases drought tolerance via abscisic acid (ABA) signaling. Because R. solanacearum-infected plants suffer reduced water flow, we hypothesized that bacterial wilt physiologically mimics drought stress, which trehalose could mitigate. We found that R. solanacearum-infected plants differentially expressed drought-associated genes, including those involved in ABA and trehalose metabolism, and had more ABA in xylem sap. Consistent with this, treating tomato roots with ABA reduced both stomatal conductance and stem colonization by R. solanacearum. Treating roots with trehalose increased xylem sap ABA and reduced plant water use by lowering stomatal conductance and temporarily improving water use efficiency. Trehalose treatment also upregulated expression of salicylic acid (SA)-dependent tomato defense genes; increased xylem sap levels of SA and other antimicrobial compounds; and increased bacterial wilt resistance of SA-insensitive NahG tomato plants. Additionally, trehalose treatment increased xylem concentrations of jasmonic acid and related oxylipins. Finally, trehalose-treated plants were substantially more resistant to bacterial wilt disease. Together, these data show that exogenous trehalose reduced both water stress and bacterial wilt disease and triggered systemic disease resistance, possibly through a Damage Associated Molecular Pattern (DAMP) response pathway. This suite of responses revealed unexpected linkages between plant responses to biotic and abiotic stress and suggested that R. solanacearum-infected plants increase trehalose to improve water use efficiency and increase wilt disease resistance. The pathogen may degrade trehalose to counter these efforts. Together, these results suggest that treating tomatoes with exogenous trehalose could be a practical strategy for bacterial wilt management.

Project description:Plant xylem fluid is considered a nutrient-poor environment, but the bacterial wilt pathogen Ralstonia solanacearum is well adapted to it, growing to 10(8) to 10(9) 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 × 10(8) 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.

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Dataset Information

Transcriptome Analysis Reveals New Insights into the Bacterial Wilt Resistance Mechanism Mediated by Silicon in Tomato.

Publications

Transcriptome Analysis Reveals New Insights into the Bacterial Wilt Resistance Mechanism Mediated by Silicon in Tomato.

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