Low environmentally relevant levels of bioactive xenobiotics and associated degradation products cause cryptic perturbations of metabolism and molecular stress responses in Arabidopsis thaliana

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Abstract

Anthropic changes and chemical pollution confront wild plant communities with xenobiotic combinations of bioactive molecules, degradation products, and adjuvants that constitute chemical challenges potentially affecting plant growth and fitness. Such complex challenges involving residual contamination and mixtures of pollutants are difficult to assess. The model plant Arabidopsis thaliana was confronted by combinations consisting of the herbicide glyphosate, the fungicide tebuconazole, the glyphosate degradation product aminomethylphosphonic acid (AMPA), and the atrazine degradation product hydroxyatrazine, which had been detected and quantified in soils of field margins in an agriculturally intensive region. Integrative analysis of physiological, metabolic, and gene expression responses was carried out in dose–response experiments and in comparative experiments of varying pesticide combinations. Field margin contamination levels had significant effects on plant growth and metabolism despite low levels of individual components and the presence of pesticide degradation products. Biochemical and molecular analysis demonstrated that these less toxic degradation products, AMPA and hydroxyatrazine, by themselves elicited significant plant responses, thus indicating underlying mechanisms of perception and transduction into metabolic and gene expression changes. These mechanisms may explain observed interactions, whether positive or negative, between the effects of pesticide products (AMPA and hydroxyatrazine) and the effects of bioactive xenobiotics (glyphosate and tebuconazole). Finally, the metabolic and molecular perturbations induced by low levels of xenobiotics and associated degradation products were shown to affect processes (carbon balance, hormone balance, antioxidant defence, and detoxification) that are likely to determine environmental stress sensitivity.

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