Title: "Polychlorinated biphenyls modify Arabidopsis root exudation pattern to accommodate degrading bacteria, showing strain and functional trait specificity".
Introduction: The importance of plant rhizodeposition to sustain microbial growth and induce xenobiotic degradation in polluted environments is increasingly recognized.
Methods: Here the “cry-for-help” hypothesis, consisting in root chemistry remodeling upon stress, was investigated in the presence of polychlorinated biphenyls (PCBs), highly recalcitrant and phytotoxic compounds, highlighting its role in reshaping the nutritional and signaling features of the root niche to accommodate PCB-degrading microorganisms.
Results: Arabidopsis exposure to 70 µM PCB-18 triggered plant-detrimental effects, stress-related traits, and PCB-responsive gene expression, reproducing PCB phytotoxicity. The root exudates of plantlets exposed for 2 days to the pollutant were collected and characterized through untargeted metabolomics analysis by liquid chromatography–mass spectrometry. Principal component analysis disclosed a different root exudation fingerprint in PCB-18-exposed plants, potentially contributing to the “cry-for-help” event. To investigate this aspect, the five compounds identified in the exudate metabolomic analysis (i.e., scopoletin, N-hydroxyethyl-b-alanine, hypoxanthine, L-arginyl-L-valine, and Lseryl-L-phenylalanine) were assayed for their influence on the physiology and functionality of the PCB-degrading strains Pseudomonas alcaliphila JAB1, Paraburkholderia xenovorans LB400, and Acinetobacter calcoaceticus P320. Scopoletin, whose relative abundance decreased in PCB-18-stressed plant exudates, hampered the growth and proliferation of strains JAB1 and P320, presumably due to its antimicrobial activity, and reduced the beneficial effect of Acinetobacter P320, which showed a higher degree of growth promotion in the scopoletin-depleted mutant f6’h1 compared to Arabidopsis WT plants exposed to PCB. Nevertheless, scopoletin induced the expression of the bph catabolic operon in strains JAB1 and LB400. The primary metabolites hypoxanthine, L-arginyl-L-valine, and L-seryl-L-phenylalanine, which increased in relative abundance upon PCB-18 stress, were preferentially used as nutrients and growth-stimulating factors by the three degrading strains and showed a variable ability to affect rhizocompetence traits like motility and biofilm formation.
Discussion: These findings expand the knowledge on PCB-triggered “cry-for-help” and its role in steering the PCB-degrading microbiome to boost the holobiont fitness in polluted environments.
CITATION: Rolli E, Ghitti E, Mapelli F and Borin S (2024) Polychlorinated biphenyls modify Arabidopsis root exudation pattern to accommodate degrading bacteria, showing strain and functional trait specificity. Front. Plant Sci. 15:1429096. doi: 10.3389/fpls.2024.1429096
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement N° 841317. E.R. thanks support from the project “SMART- Exploring the seed microbiome in polluted soil for bioremediation and agricultural applications” (PSR2022: Linea 2- Azione A, Università degli Studi di Milano). The authors thank support from the European Union’s Horizon 2020 project NYMPHE. NYMPHE is a project funded by the European Union’s Horizon Europe – Research and Innovation funding programme (2021 - 2027), under Grant agreement n. 101060625 (https://www.nympheproject.eu/). Views and opinions expressed are however those of the author(s) only and do not necessarily reflect those of the European Union. Neither the European Union nor the granting authority can be held responsible for them.
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