Identification of a dioxin-responsive oxylipin signature in roots of date palm: involvement of a 9-hydroperoxide fatty acid reductase, caleosin/peroxygenase PdPXG2

Abstract

Dioxins are highly hazardous pollutants that have well characterized impacts on both animal and human health. However, the biological effects of dioxins on plants have yet to be described in detail. Here we describe a dioxin-inducible caleosin/peroxygenase isoform, PdPXG2, that is mainly expressed in the apical zone of date palm roots and specifically reduces 9-hydroperoxide fatty acids. A characteristic spectrum of 18 dioxin-responsive oxylipin (DROXYL) congeners was also detected in date palm roots after exposure to dioxin. Of particular interest, six oxylipins, mostly hydroxy fatty acids, were exclusively formed in response to TCDD. The DROXYL signature was evaluated in planta and validated in vitro using a specific inhibitor of PdPXG2 in a root-protoplast system. Comparative analysis of root suberin showed that levels of certain monomers, especially the mono-epoxides and tri-hydroxides of C16:3 and C18:3, were significantly increased after exposure to TCDD. Specific inhibition of PdPXG2 activity revealed a positive linear relationship between deposition of suberin in roots and their permeability to TCDD. The results highlight the involvement of this peroxygenase in the plant response to dioxin and suggest the use of dioxin-responsive oxylipin signatures as biomarkers for plant exposure to this important class of xenobiotic contaminants.

Dioxin impacts on lipid metabolism of soil microbes: towards effective detection and bioassessment strategies

“…In connection with exposure to dioxin, TCDD-exposed fungi expressed more AfPXG and accumulated more LDs than controls, which probably aids the fungal cells to sequester dioxin into LDs. Similar induction of caleosin isoforms was also reported in plants experimentally exposed to TCDD (Hanano et al 2016b(Hanano et al , 2018d. These data highlight the possible effects of dioxins on aflatoxicogenicity of A. flavus.…”

“…However, even leafy crops can be exposed to dioxins indirectly from contaminated soil due to their active root systems (Hanano et al 2014b(Hanano et al , 2018b. Longer lived perennial and woody plants can accumulate considerable amount of dioxins from the surrounding atmosphere as well as via their well-developed root systems (Hanano et al 2016b(Hanano et al , 2018d. More research is needed to define and evaluate the modalities by which plants can be exposed to dioxins, compared to animals that are directly exposed via contaminated feed (Torres et al 2013;Diletti et al 2007).…”

“…Oxygenated FAs, also termed oxylipins, are well known as essential molecules enabling animals, plants and microorganisms to respond to various forms of biotic and abiotic stress (Mohammadpour et al 1988;Bestervelt et al 1994;Hanano et al 2018d). In microorganisms, oxylipins play crucial roles in regulating the biosynthesis of secondary metabolite (Hanano et al 2018a(Hanano et al , 2019a, as well as the production of biosurfactants and their emulsifying activity towards hydrophobic compounds (Hanano et al 2014a(Hanano et al , 2015c(Hanano et al , 2017(Hanano et al , 2019b.…”

“…Oxylipins have also roles in altering bacterial membrane fluidity as a function of environmental stress (Denich et al 2003). For these reasons, the signatures of the various FAs and their metabolites have been proposed to be used as biomarkers for biomonitoring the exposure of animals, plants and soil microorganisms to dioxins (Hiraishi et al 2003a;Bassompierre et al 2007;Hanano et al 2018dHanano et al , 2019b.…”

Identification of a caleosin associated with hazelnut (Corylus avellana L.) oil bodies

“…Interestingly, two caleosin/peroxygenase isoforms from date palm (PdCLO2/PdPXG2 and PdCLO4/PdPXG4), associated with the OB and microsomal fractions, were characterized with respect to their tissue localization, temporal expression and oxylipin pathway substrate specificities (Hanano et al ). In addition, the involvement of PdPXC2, which reduces 9‐hydroperoxide fatty acids, in the root response to exposure to dioxin, which is an environmental contaminant, has been suggested (Hanano et al ). However, how these proteins interact with OB to generate peroxygenase‐derived lipid metabolites or influence other signalling components in plant cells still remains to be determined (Huang ).…”