Abstract
Polychlorinated biphenyls (PCBs) are persistent organic pollutants with severe effects on human health and the biosphere. Plant-based remediation offers many benefits over conventional PCB remediation, but its development has been hampered by our poor understanding of biphenyl metabolism in eukaryotes, among other factors. We report here a major PCB-responsive protein in poplar, a plant model system capable of PCB uptake and translocation. We provide structural and functional evidence that this uncharacterized protein, termed SDR57C, belongs to the heterogeneous short-chain dehydrogenase reductase (SDR) superfamily. Despite sequence divergence, structural modeling hinted at structural and functional similarities between SDR57C and BphB, a central component of the Bph pathway for biphenyl/PCB degradation in aerobic bacteria. By combining gas chromatography/mass spectrometry (GC/MS) profiling with a functional complementation scheme, we found that poplar SDR57C can replace BphB activity in the upper Bph pathway of Pseudomonas furukawaii KF707 and therefore catalyze the oxidation of 2,3-dihydro-2,3-dihydroxybiphenyl (2,3-DHDB) to 2,3-dihydroxybiphenyl (2,3-DHB). Consistent with this biochemical activity, we propose a mechanism of action based on prior quantum studies, general properties of SDR enzymes, and the modeled docking of 2,3-DHDB to the SDR57C-NAD+ complex. The putative detoxifying capacity of SDR57C was substantiated through reverse genetics in Arabidopsis thaliana Phenotypic characterization of the SDR lines underscored an inducible plant pathway with the potential to catabolize toxic biphenyl derivatives. Partial similarities with aerobic bacterial degradation notwithstanding, real-time messenger RNA quantification indicates the occurrence of plant-specific enzymes and features. Our results may help explain differences in degradative abilities among plant genotypes and also provide elements to improve them.
Highlights
Polychlorinated biphenyls (PCBs) are persistent organic pollutants with severe effects on human health and the biosphere
Accumulation of two major responsive leaf polypeptides was consistently detected in Populus tremula x Populus alba plants exposed to PCB mixtures but not in plants exposed to the PCB solvent alone (Fig. 1A)
The catalytic residues of BphBLB400, Tyr155, and Lys159, are spatially matched in SDR57C by Tyr199 and Lys203 (Fig. 1D). These findings strongly suggest that poplar SDR57C may directly attack biphenyl moieties in the same manner as BphB enzymes
Summary
Polychlorinated biphenyls (PCBs) are persistent organic pollutants with severe effects on human health and the biosphere. By combining gas chromatography/mass spectrometry (GC/MS) profiling with a functional complementation scheme, we found that poplar SDR57C can replace BphB activity in the upper Bph pathway of Pseudomonas furukawaii KF707 and catalyze the oxidation of 2,3-dihydro-2,3-dihydroxybiphenyl (2,3-DHDB) to 2,3-dihydroxybiphenyl (2,3-DHB) Consistent with this biochemical activity, we propose a mechanism of action based on prior quantum studies, general properties of SDR enzymes, and the modeled docking of 2,3-DHDB to the SDR57C-NAD+ complex. By integrating functional and structural studies, we define here a plant-specific pathway which is activated by and possibly contributes to detoxifying biphenyl-derived toxicants. This pathway exhibits common features with bacterial biphenyl/PCB degradation and significant differences. These plant enzymes show little or no sequence similarity with their bacterial “counterparts.” Taken together, our results indicate the existence of a plant-specific pathway for biphenyl/PCB catabolism
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