Chloroplast-derived photo-oxidative stress causes changes in H2O2 and EGSH in other subcellular compartments

Ugalde, J. M.; Fuchs, P.; Nietzel, T.; Cutolo, E.; Vothknecht, U. C.; Holuigue, L.; Schwarzländer, M.; Müller-Schüssele, S. J.; Meyer, A. J.

doi:10.1101/2020.07.20.212670

bioRxiv · 10.1101/2020.07.20.212670

Chloroplast-derived photo-oxidative stress causes changes in H2O2 and EGSH in other subcellular compartments

Ugalde, J. M.·Fuchs, P.·Nietzel, T.·Cutolo, E.·Vothknecht, U. C.·Holuigue, L.·Schwarzländer, M.·Müller-Schüssele, S. J.·Meyer, A. J.

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Abstract

Metabolic fluctuations in chloroplasts and mitochondria can trigger retrograde signals to modify nuclear gene expression. Mobile signals likely to be involved are reactive oxygen species (ROS), which can operate protein redox switches by oxidation of specific cysteine residues. Redox buffers such as the highly reduced glutathione pool serve as reservoirs of reducing power for several ROS scavenging and ROS-induced damage repair pathways. Formation of glutathione disulfide (GSSG) and a shift of the glutathione redox potential (EGSH) towards less negative values is considered a hallmark of several stress conditions. Here we used the herbicide methyl viologen (MV) to generate ROS locally in chloroplasts of intact Arabidopsis seedlings and recorded dynamic changes in EGSH and H2O2 levels with the genetically-encoded biosensors Grx1-roGFP2 (for EGSH) and roGFP2-Orp1 (for H2O2) targeted to chloroplasts, the cytosol or mitochondria. Treatment of seedlings with MV caused a rapid oxidation in chloroplasts and subsequently also in the cytosol and mitochondria. The MV-induced oxidation was significantly boosted by illumination with actinic light and largely abolished by inhibitors of photosynthetic electron transport. In addition, MV also induced an autonomous oxidation in the mitochondrial matrix in an electron transport chain activity-dependent manner that was milder than the oxidation triggered in chloroplasts by the combination of MV and light. In vivo redox biosensing resolves the spatiotemporal dynamics of compartmental responses to local ROS generation and provide a basis for understanding how compartment-specific redox dynamics may operate in retrograde signaling and stress acclimation in plants. One sentence summaryMethyl viologen-induced photooxidative stress causes an increase of H2O2 and oxidation of glutathione in chloroplasts, cytosol and mitochondria as well as autonomous oxidation in mitochondria.

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Ugalde, J. M., Fuchs, P., Nietzel, T., Cutolo, E., Vothknecht, U. C., Holuigue, L., Schwarzländer, M., Müller-Schüssele, S. J., Meyer, A. J.. 2020-07-23. Chloroplast-derived photo-oxidative stress causes changes in H2O2 and EGSH in other subcellular compartments. https://doi.org/10.1101/2020.07.20.212670

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