Evolutionary Conserved and Divergent Responses to Copper Zinc Superoxide Dismutase Inhibition in Plants

After an initial evolution in a reducing environment, life got successively challenged by reactive oxygen species (ROS), especially during the great oxidation event (GOE) that followed the development of photosynthesis. Therefore, ROS are deeply intertwined into the physiological, morphological and transcriptional responses of most present-day organisms. Copper-zinc superoxide dismutases (CuZnSODs) evolved during the GOE and are present in charophytes and extant land plants, but nearly absent from chlorophytes. The chemical inhibitor of CuZnSOD, lung cancer screen 1 (LCS-1), could greatly facilitate the study of SODs in diverse plants. Here, we determined the impact of chemical inhibition of plant CuZnSOD activity, on plant growth, transcription and metabolism. We followed a comparative approach by using different plant species, including Marchantia Polymorpha and Physcomitrium patens, representing bryophytes, the sister lineage to vascular plants, and Arabidopsis thaliana. We show that LCS-1 causes oxidative stress in plants and that the inhibition of CuZnSODs provoked a similar core response that mainly impacted glutathione homoeostasis in all plant species analysed. That said, Physcomitrium and Arabidopsis, which contain multiple CuZnSOD isoforms showed a more complex and exacerbated response. In addition, an untargeted metabolomics approach revealed a specific metabolic signature for each plant species. Our comparative analysis exposes a conserved core response at the physiological and transcriptional level towards LCS-1, while the metabolic response largely varies. These differences correlate with the number and localization of the CuZnSOD isoforms present in each species.