Unraveling the early molecular and physiological mechanisms involved in response to phenanthrene exposure

Abstract

BackgroundHigher plants have to cope with increasing concentrations of pollutants of both natural and anthropogenic origin. Given their capacity to concentrate and metabolize various compounds including pollutants, plants can be used to treat environmental problems - a process called phytoremediation. However, the molecular mechanisms underlying the stabilization, the extraction, the accumulation and partial or complete degradation of pollutants by plants remain poorly understood.ResultsHere, we determined the molecular events involved in the early plant response to phenanthrene, used as a model of polycyclic aromatic hydrocarbons. A transcriptomic and a metabolic analysis strongly suggest that energy availability is the crucial limiting factor leading to high and rapid transcriptional reprogramming that can ultimately lead to death. We show that the accumulation of phenanthrene in leaves inhibits electron transfer and photosynthesis within a few minutes, probably disrupting energy transformation.ConclusionThis kinetic analysis improved the resolution of the transcriptome in the initial plant response to phenanthrene, identifying genes that are involved in primary processes set up to sense and detoxify this pollutant but also in molecular mechanisms used by the plant to cope with such harmful stress. The identification of first events involved in plant response to phenanthrene is a key step in the selection of candidates for further functional characterization, with the prospect of engineering efficient ecological detoxification systems for polycyclic aromatic hydrocarbons.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3133-0) contains supplementary material, which is available to authorized users.

Transcriptome response of the foundation plant Spartina alterniflora to the Deepwater Horizon oil spill

“…Of these “super‐responsive” A. thaliana genes, 85 gene homologs (including six from the xenome) in S. alterniflora were also responsive to the DWH crude oil, highlighting the potential importance of this small subset of genes in a diverse array of responses that may be functionally conserved across taxa. In addition, 149 “stress annotation” genes responded in at least one of the previous A. thaliana phenanthrene studies, including 18 “super responders,” all of which also responded in S. alterniflora (Supporting information File ; Dumas et al., ; Weisman et al., ).…”

“…() and Dumas et al. () studies. We then compared only the loci whose homologs were present on the Spartina array and were also represented on either the ATH1 or the CATMA.…”

“…Dumas et al. () ran a time series experiment exposing 15‐day‐old seedlings to phenanthrene for 30 min, 2, 4, 8 and 24 hr identifying 467 genes that responded to phenanthrene in at least one of these time points. Combined, these studies captured gene expression response to phenanthrene that was affected in either the short term or the long‐term in 1,426 genes.…”

“…() study or the Dumas et al. () study. To facilitate the comparison with S. alterniflora , we only used genes that appeared on the custom S. alterniflora microarray and on either the ATH1 or CATMA chips.…”

“…(a) Simplified scheme of metabolic pathways of xenobiotic (X) detoxification in plant cells: The thick line indicates the cell membrane, and xenome components are indicated in red. (b) The total number of xenome genes expressed in S. alterniflora in response to oil contamination in the field, compared to those observed for Col‐0 shoot tissue in response to the PAH phenanthrene (Dumas et al., ; Weisman et al., ). (c) Graphical matrix depicting differentially expressed xenome loci in response to phenanthrene in A. thaliana (Dumas et al., ; Weisman et al., ), and in response to the DWH oil spill in S. alterniflora .…”