Abstract

In the present work, we used a double cell screening approach based on phenanthrene (phe) epifluorescence histochemical localization and oxygen radical detection to generate new data about how some specialized cells are involved in tolerance to organic xenobiotics. Thereby, we bring new insights about phe [a common Polycyclic Aromatic Hydrocarbon (PAH)] cell specific detoxification, in two contrasting plant lineages thriving in different ecosystems. Our data suggest that in higher plants, detoxification may occur in specialized cells such as trichomes and pavement cells in Arabidopsis, and in the basal cells of salt glands in Spartina species. Such features were supported by a survey from the literature, and complementary data correlating the size of basal salt gland cells and tolerance abilities to PAHs previously reported between Spartina species. Furthermore, we conducted functional validation in two independent Arabidopsis trichomeless glabrous T-DNA mutant lines (GLABRA1 mutants). These mutants showed a sensitive phenotype under phe-induced stress in comparison with their background ecotypes without the mutation, indicating that trichomes are key structures involved in the detoxification of organic xenobiotics. Interestingly, trichomes and pavement cells are known to endoreduplicate, and we discussed the putative advantages given by endopolyploidy in xenobiotic detoxification abilities. The same feature concerning basal salt gland cells in Spartina has been raised. This similarity with detoxification in the endopolyploid liver cells of the animal system is included.

Highlights

  • Worldwide environmental accumulation of organic xenobiotics is a major concern for natural ecosystems and public health

  • We performed both cellular localization of phe and oxidative stress markers in Arabidopsis and Spartina to assess the putative role of specialized cells in xenobiotic detoxification strategies

  • Arabidopsis plantlets were grown under control and moderate phe (25 μm) conditions, and leaves were filtered under vacuum with Singlet Oxygen Sensor Green (SOSG)

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Summary

Introduction

Worldwide environmental accumulation of organic xenobiotics is a major concern for natural ecosystems and public health. Organic xenobiotic metabolization and transformation by plants remain incompletely characterized, a model has been proposed (Edwards et al, 2005; Edwards et al, 2011; El Amrani et al, 2015; Sun et al, 2019) with three major steps: (1) signaling, (2) transport and transformation, and (3) compartmentalization. This model involves a myriad of enzymes from the xenome, among alpha-beta hydrolases (e.g. peroxidases and esterases) and cytochromes P450 (CYPs) for xenobiotic hydroxylation acting on their solubility, and glutathione-S-transferases (GSTs), glycosyltransferases (GTs), and malonyltransferases (MTs) for xenobiotic conjugation with endogenous glutathione, glycosyl or malonyl groups, respectively. Oxidative stress damages related with reactive oxygen species (ROS) accumulation under abiotic stress are most likely limiting plant tolerance abilities (Liu et al, 2009)

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