Lipopolysaccharides from Ralstonia solanacearum induce a broad metabolomic response in Solanum lycopersicum

Dylan R Zeiss; Antonio Molinaro; Paul A Steenkamp; Alba Silipo; Lizelle A Piater; Flaviana Di Lorenzo; Ian A Dubery

doi:10.3389/fmolb.2023.1232233

Lipopolysaccharides from Ralstonia solanacearum induce a broad metabolomic response in Solanum lycopersicum

Front Mol Biosci. 2023 Aug 10:10:1232233. doi: 10.3389/fmolb.2023.1232233. eCollection 2023.

Authors

Dylan R Zeiss¹, Antonio Molinaro^{2

3}, Paul A Steenkamp¹, Alba Silipo^{2

3}, Lizelle A Piater¹, Flaviana Di Lorenzo^{2

3}, Ian A Dubery¹

Affiliations

¹ Research Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Auckland Park, South Africa.
² Department of Chemical Sciences, University of Napoli Federico II, Complesso Universitario Monte Sant'Angelo, Naples, Italy.
³ Task Force on Microbiome Studies, University of Napoli Federico II, Complesso Universitario Monte Sant'Angelo, Naples, Italy.

Abstract

Ralstonia solanacearum, one of the most destructive crop pathogens worldwide, causes bacterial wilt disease in a wide range of host plants. The major component of the outer membrane of Gram-negative bacteria, lipopolysaccharides (LPS), has been shown to function as elicitors of plant defense leading to the activation of signaling and defense pathways in several plant species. LPS from a R. solanacearum strain virulent on tomato (LPS_{R. sol.}), were purified, chemically characterized, and structurally elucidated. The lipid A moiety consisted of tetra- to hexa-acylated bis-phosphorylated disaccharide backbone, also decorated by aminoarabinose residues in minor species, while the O-polysaccharide chain consisted of either linear tetrasaccharide or branched pentasaccharide repeating units containing α-L-rhamnose, N-acetyl-β-D-glucosamine, and β-L-xylose. These properties might be associated with the evasion of host surveillance, aiding the establishment of the infection. Using untargeted metabolomics, the effect of LPS_{R. sol.} elicitation on the metabolome of Solanum lycopersicum leaves was investigated across three incubation time intervals with the application of UHPLC-MS for metabolic profiling. The results revealed the production of oxylipins, e.g., trihydroxy octadecenoic acid and trihydroxy octadecadienoic acid, as well as several hydroxycinnamic acid amide derivatives, e.g., coumaroyl tyramine and feruloyl tyramine, as phytochemicals that exhibit a positive correlation to LPS_{R. sol.} treatment. Although the chemical properties of these metabolite classes have been studied, the functional roles of these compounds have not been fully elucidated. Overall, the results suggest that the features of the LPS_{R. sol.} chemotype aid in limiting or attenuating the full deployment of small molecular host defenses and contribute to the understanding of the perturbation and reprogramming of host metabolism during biotic immune responses.

Keywords: Solanum lycopersicum; hydroxycinnamic acid amides; lipopolysaccharides; metabolomics; oxylipins; phenylpropanoids; plant immunity.

Grants and funding

Funding from the South African National Research Foundation to ID (grant number 95818) supported the research. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. FL acknowledges the European Research Council (ERC) under the Horizon Europe program under grant agreement no. 101039841 (DEBUGGING LPS).