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.
Highlights
Termed dioxins, the polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs), are collectively the most toxic group of Persistent Organic Pollutants (POPs) that have been described to date[1]
Phylogenetic analysis confirmed that PdPXG2 clusters in the same branches as AtPXG5 and AtPXG4 (Fig. 1B) and the predicted 3D-structure of the PdPXG2 protein shows a domain configuration which significantly matches that of other plant caleosins (Fig. 1C)
PdPXG2 is most abundant in microsomes (M), less so in lipid droplets (LDs), and was absent from supernatant (S) fractions isolated from roots of date palm seedlings compared with the respective fractions isolated from leaves (Fig. 1D)
Summary
Termed dioxins, the polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs), are collectively the most toxic group of Persistent Organic Pollutants (POPs) that have been described to date[1]. Congeners with chlorine atoms positioned in 2, 3, 7 and 8 of the aromatic rings are the most toxic and 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD), with a toxic equivalency factor (TEF) of 1.0, is by far the most toxic of all the dioxins[4,5] Because they are so chemically stable, dioxins can persist in the environment and bioaccumulate in many different organisms in a given ecosystem, including bacteria, fungi, plants, insects, and larger animals including humans[6,7,8,9]. Plant and fungal caleosins/peroxygenases have distinctive features, including, a single highly conserved calcium binding, EF-hand motif plus an invariant heme-binding histidine residue in the region proximal to the N terminus This is followed by a relatively hydrophobic, potentially membrane-spanning, region plus a proline rich domain in the centre of the protein. There is a region containing several predicted kinase sites proximal to the C terminus[25,29,30,31]
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