ROS Production and Scavenging under Anoxia and Re-Oxygenation in Arabidopsis Cells: A Balance between Redox Signaling and Impairment.

Annalisa Paradiso,Laura De Gara,Rossella Nisi,Anna Bove,Antonella Leone,Sofia Caretto

doi:10.3389/fpls.2016.01803

Abstract

Plants can frequently experience low oxygen concentrations due to environmental factors such as flooding or waterlogging. It has been reported that both anoxia and the transition from anoxia to re-oxygenation determine a strong imbalance in the cellular redox state involving the production of reactive oxygen species (ROS) and nitric oxide (NO). Plant cell cultures can be a suitable system to study the response to oxygen deprivation stress since a close control of physicochemical parameters is available when using bioreactors. For this purpose, Arabidopsis cell suspension cultures grown in a stirred bioreactor were subjected to a severe anoxic stress and analyzed during anoxia and re-oxygenation for alteration in ROS and NO as well as in antioxidant enzymes and metabolites. The results obtained by confocal microscopy showed the dramatic increase of ROS, H2O2, and NO during the anoxic shock. All the ascorbate-glutathione related parameters were altered during anoxia but restored during re-oxygenation. Anoxia also induced a slight but significant increase of α-tocopherol levels measured at the end of the treatment. Overall, the evaluation of cell defenses during anoxia and re-oxygenation in Arabidopsis cell cultures revealed that the immediate response involving the overproduction of reactive species activated the antioxidant machinery including ascorbate-glutathione system, α-tocopherol and the ROS-scavenging enzymes ascorbate peroxidase, catalase, and peroxidase making cells able to counteract the stress toward cell survival.

Highlights

Plants being aerobic organisms need oxygen as an essential substrate for energy production
A rise in reactive oxygen and nitrogen species during anoxia and the activation of antioxidant system during re-oxygenation is shown in Arabidopsis cell suspensions grown in a bioreactor, which allowed the close control of oxygen levels
Since no significant differences were observed between control and treated cells, cell viability was not affected by anoxia followed by re-oxygenation

Summary

Introduction

Plants being aerobic organisms need oxygen as an essential substrate for energy production. The poor distribution efficiency for oxygen through plant organs or high rates of cellular metabolism in dividing meristem cells can induce a severe drop of plant internal oxygen concentrations. Oxygen deprivation stress in plant cells includes three different states characterized by different oxygen concentrations: hypoxia, anoxia, and reoxygenation. The responses to oxygen deprivation include various alterations of plant metabolism aimed at plant survival such as energy preservation, reduction of respiration, and induction of fermentation which occurs when oxygen levels are close to zero (Geigenberger, 2003). An oxygen sensing mechanism involving specific transcription factors, able to trigger the plant molecular response to hypoxia was identified (Licausi et al, 2011; Sasidharan and Mustroph, 2011)

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Conclusion