Metabolomic changes in Arabidopsis thaliana exposed to extracellular self- and nonself-DNA: A reversible effect

Untargeted metabolomics analysis was used to assess at molecular level the plant reactions to extracellular DNA (exDNA) exposure. Thus, the effects on the metabolites profile of A. thaliana after exposure to self- and nonself-DNA have been investigated by NMR, LC-MS and chemometrics analyses. Results confirmed that self-DNA significantly induces the accumulation of different RNA constituents along with their cyclic analogues, in form of cyclic dimers, as well as methylated forms, increasing only in the self-DNA treatment. In addition, a deeper investigation of these samples showed the increase of several metabolites belonging to the classes of indoles, flavonoids, thiazoles and isothiocyanates. All these metabolites are known to be involved in plant growth and defence. Among these, isothiocyanates are known to affect the A. thaliana cell cycle with accumulation of cells in S-phase which is consistent with observations of self-DNA inhibition in other model organisms. Noteworthy, the early metabolomic changes induced by self-DNA were shown to be reversible when followed by a second exposure to extracellular nonself-DNA. These results highlight the relevance of the environmental balance between self- and nonself-DNA in the regulation of plant metabolism. Arabidopsis thaliana exposed to extracellular self-DNA increases the production of specific metabolites belonging to nucleotides, indoles, flavonoids, thiazoles, isothiocyanates. Exposure to nonself-DNA increases amino acids. The inhibitory effect of self-DNA is reversible after exposure to nonself-DNA • Arabidopsis thaliana metabolites after self- and nonself-DNA exposure are analysed. • Significant accumulation of ribonucleotides after self-DNA exposure is confirmed. • Extracellular self-DNA increases indoles, flavonoids, thiazoles and isothiocyanates. • Extracellular nonself-DNA increases amino acids content. • The inhibitory effect of self-DNA is reversible after exposure to nonself-DNA.

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Publication Details

Journal
Environmental and Experimental Botany
Published
2025-04-21
DOI
https://doi.org/10.1016/j.envexpbot.2025.106149
Citations
2
Primary Topic
Photosynthetic Processes and Mechanisms
Type
article
Field-Weighted Citation Impact
1.61
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article

Metabolomic changes in Arabidopsis thaliana exposed to extracellular self- and nonself-DNA: A reversible effect

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2 citations
Environmental and Experimental Botany
Photosynthetic Processes and Mechanisms
1.61
article

Metabolomic changes in Arabidopsis thaliana exposed to extracellular self- and nonself-DNA: A reversible effect

Pasquale Termolino, Alfonso Mangoni, Stefano Mazzoleni, Laura Grauso, Bruna de Falco, Fabrizio Cartenì, Virginia Lanzotti, Emanuela Palomba
article en
2 citations

Abstract

Untargeted metabolomics analysis was used to assess at molecular level the plant reactions to extracellular DNA (exDNA) exposure. Thus, the effects on the metabolites profile of A. thaliana after exposure to self- and nonself-DNA have been investigated by NMR, LC-MS and chemometrics analyses. Results confirmed that self-DNA significantly induces the accumulation of different RNA constituents along with their cyclic analogues, in form of cyclic dimers, as well as methylated forms, increasing only in the self-DNA treatment. In addition, a deeper investigation of these samples showed the increase of several metabolites belonging to the classes of indoles, flavonoids, thiazoles and isothiocyanates. All these metabolites are known to be involved in plant growth and defence. Among these, isothiocyanates are known to affect the A. thaliana cell cycle with accumulation of cells in S-phase which is consistent with observations of self-DNA inhibition in other model organisms. Noteworthy, the early metabolomic changes induced by self-DNA were shown to be reversible when followed by a second exposure to extracellular nonself-DNA. These results highlight the relevance of the environmental balance between self- and nonself-DNA in the regulation of plant metabolism. Arabidopsis thaliana exposed to extracellular self-DNA increases the production of specific metabolites belonging to nucleotides, indoles, flavonoids, thiazoles, isothiocyanates. Exposure to nonself-DNA increases amino acids. The inhibitory effect of self-DNA is reversible after exposure to nonself-DNA • Arabidopsis thaliana metabolites after self- and nonself-DNA exposure are analysed. • Significant accumulation of ribonucleotides after self-DNA exposure is confirmed. • Extracellular self-DNA increases indoles, flavonoids, thiazoles and isothiocyanates. • Extracellular nonself-DNA increases amino acids content. • The inhibitory effect of self-DNA is reversible after exposure to nonself-DNA.

Environmental and Experimental BotanyVol. 234
Institute of Biosciences and Bioresources (IT), Federico II University Hospital (IT), University of Naples Federico II (IT)
Zero hunger
Openalex Percentile: Top 18%
Photosynthetic Processes and Mechanisms
1.61
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