Abstract
A highly negative glutathione redox potential (EGSH ) is maintained in the cytosol, plastids and mitochondria of plant cells to support fundamental processes, including antioxidant defence, redox regulation and iron-sulfur cluster biogenesis. Out of two glutathione reductase (GR) proteins in Arabidopsis, GR2 is predicted to be dual-targeted to plastids and mitochondria, but its differential roles in these organelles remain unclear. We dissected the role of GR2 in organelle glutathione redox homeostasis and plant development using a combination of genetic complementation and stacked mutants, biochemical activity studies, immunogold labelling and in vivo biosensing. Our data demonstrate that GR2 is dual-targeted to plastids and mitochondria, but embryo lethality of gr2 null mutants is caused specifically in plastids. Whereas lack of mitochondrial GR2 leads to a partially oxidised glutathione pool in the matrix, the ATP-binding cassette (ABC) transporter ATM3 and the mitochondrial thioredoxin system provide functional backup and maintain plant viability. We identify GR2 as essential in the plastid stroma, where it counters GSSG accumulation and developmental arrest. By contrast a functional triad of GR2, ATM3 and the thioredoxin system in the mitochondria provides resilience to excessive glutathione oxidation.
Highlights
The use of oxygen by aerobic organisms allows them to obtain more energy from carbohydrates, by accessing a larger reduction potential difference
While we found that Arabidopsis mutants lacking cytosolic GR1 are fully viable (Marty et al, 2009), a deletion mutant lacking functional GR2 is embryo lethal (Tzafrir et al, 2004; Bryant et al, 2011; Ding et al, 2016b)
Using a series of physiological and genetic analyses we identify the involvement of alternative GSSG reduction systems and of GSSG export in EGSH maintenance in the mitochondrial matrix
Summary
The use of oxygen by aerobic organisms allows them to obtain more energy from carbohydrates, by accessing a larger reduction potential difference. Other metabolic reactions in the cell, lead to reduction of oxygen and give rise to reactive oxygen species (ROS), such as superoxide (O2À), hydrogen peroxide (H2O2) and hydroxyl radicals. Low levels of ROS have been implicated in signalling between subcellular compartments as well as long-distance signalling regulating plant development and metabolism (Foyer & Noctor, 2009; Gilroy et al, 2016). ROS constitute a major threat to the cell and need to be tightly controlled. Overreduction of the electron transport chain results in O2À production at complexes I and III (Moller, 2001). In both compartments, O2À quickly dismutates to H2O2 and O2 in a reaction catalysed by superoxide dismutase (SOD)
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