From Endoplasmic Reticulum to Mitochondria: Absence of the Arabidopsis ATP Antiporter Endoplasmic Reticulum Adenylate Transporter1 Perturbs Photorespiration

Abstract

The carrier Endoplasmic Reticulum Adenylate Transporter1 (ER-ANT1) resides in the endoplasmic reticulum (ER) membrane and acts as an ATP/ADP antiporter. Mutant plants lacking ER-ANT1 exhibit a dwarf phenotype and their seeds contain reduced protein and lipid contents. In this study, we describe a further surprising metabolic peculiarity of the er-ant1 mutants. Interestingly, Gly levels in leaves are immensely enhanced (263) when compared with that of wild-type plants. Gly accumulation is caused by significantly decreased mitochondrial glycine decarboxylase (GDC) activity. Reduced GDC activity in mutant plants was attributed to oxidative posttranslational protein modification induced by elevated levels of reactive oxygen species (ROS). GDC activity is crucial for photorespiration; accordingly, morphological and physiological defects in er-ant1 plants were nearly completely abolished by application of high environmental CO 2 concentrations. The latter observation demonstrates that the absence of ER-ANT1 activity mainly affects photorespiration (maybe solely GDC), whereas basic cellular metabolism remains largely unchanged. Since ER-ANT1 homologs are restricted to higher plants, it is tempting to speculate that this carrier fulfils a plant-specific function directly or indirectly controlling cellular ROS production. The observation that ER-ANT1 activity is associated with cellular ROS levels reveals an unexpected and critical physiological connection between the ER and other organelles in plants.

Independent and Parallel Evolution of New Genes by Gene Duplication in Two Origins of C4 Photosynthesis Provides New Insight into the Mechanism of Phloem Loading in C4 Species

“…2A and 2 B , Supplementary Material online). Glutaredoxin genes are involved in antioxidant defense and stimulate photorespiratory glycine decarboxylase activity in plant mitochondria ( Hoffmann et al 2013 ). Thus given the expression of the duplicate genes in BS cells, it is possible that they function to protect the cell from oxidative damage as a result of activation of photosynthesis.…”

Redox-Regulation of Photorespiration through Mitochondrial Thioredoxin o1

“…To date, a redox-regulation mechanism was proposed and experimentally verified only for the Synechocystis GDC P-protein (Hasse et al, 2013), the actual Gly decarboxylase. It has also been shown that the entire GDC activity became severely inhibited in a more oxidized and reactive oxygen speciesproducing mitochondrion due to a defect in the endoplasmic reticulum-localized adenylate transporter 1 (ER-ANT1) in Arabidopsis and rice (Oryza sativa;Hoffmann et al, 2013;Zhang et al, 2016), which was partly relieved upon DTT addition (Hoffman et al, 2013). These findings stimulated us to test GDC-L (mtLPD) for its potential to undergo redox-regulation, which could be based on disulfide bond formation that has been in silico predicted onto the LPD structure (Faure et al, 2000).…”

The Roles of Mitochondrial Reactive Oxygen Species in Cellular Signaling and Stress Response in Plants

“…The reverse, i.e. H 2 O 2 produced by the ER to be sensed within the mitochondrial matrix inducing glutathionylation of a Gly decarboxylase subunit, has been proposed recently (Hoffmann et al, 2013). A recent study suggests that the twin-Cys proteins At12cys1/2 can relocate from the mitochondria to cytosol and chloroplast upon Complex I dysfunction, providing a potential mechanism to signal mitochondrial dysfunction to the rest of the cell in plants (Wang et al, 2016).…”