Nitrogen Source Dependent Changes in Central Sugar Metabolism Maintain Cell Wall Assembly in Mitochondrial Complex I-Defective frostbite1 and Secondarily Affect Programmed Cell Death

Abstract

For optimal plant growth, carbon and nitrogen availability needs to be tightly coordinated. Mitochondrial perturbations related to a defect in complex I in the Arabidopsis thaliana frostbite1 (fro1) mutant, carrying a point mutation in the 8-kD Fe-S subunit of NDUFS4 protein, alter aspects of fundamental carbon metabolism, which is manifested as stunted growth. During nitrate nutrition, fro1 plants showed a dominant sugar flux toward nitrogen assimilation and energy production, whereas cellulose integration in the cell wall was restricted. However, when cultured on NH4+ as the sole nitrogen source, which typically induces developmental disorders in plants (i.e., the ammonium toxicity syndrome), fro1 showed improved growth as compared to NO3− nourishing. Higher energy availability in fro1 plants was correlated with restored cell wall assembly during NH4+ growth. To determine the relationship between mitochondrial complex I disassembly and cell wall-related processes, aspects of cell wall integrity and sugar and reactive oxygen species signaling were analyzed in fro1 plants. The responses of fro1 plants to NH4+ treatment were consistent with the inhibition of a form of programmed cell death. Resistance of fro1 plants to NH4+ toxicity coincided with an absence of necrotic lesion in plant leaves.

Glyoxalase I activity affects Arabidopsis sensitivity to ammonium nutrition

“…DJ-1 may also serve a similar function in plants because it has been shown that Arabidopsis insertional mutants possessing elevated DJ-1A levels are characterized by increased protection against environmental stress conditions achieved through DJ-1A-dependent activation of ROS-quenching enzymes, including superoxide dismutase 1 (SOD1) and glutathione peroxidase 2 (GPX2) (Xu et al 2010 ), or interaction with ascorbate peroxidase 1 (APX1) (Xu and Møller 2010 ). Arabidopsis DJ-1A is localized to the cytosol and the nucleus (Xu et al 2010 ) and its upregulated expression may be related to an increased demand for enhanced antioxidant capacity under ammonium feeding conditions when oxidative stress occurs (Podgórska et al 2018a , b ). Although DJ-1D displays the most distinct glyoxalase activity among all the DJ-1 proteins (Kwon et al 2013 ), neither upregulation of DJ-1D by ammonium (Fig.…”

“…7 d) and were more resistant to exogenous d -lactate (K. Borysiuk, B. Szal, results not presented). Such a feature seems not to be a simple consequence of the differences in the level of electron acceptor for reaction by d -LDH since cytochrome c (cyt c ) levels are lower in ammonium-grown fro1 plants than in WT plants (Podgórska et al 2018a , b ). However, d -LDH function requires oxidized cyt c availability, and its level depends on the electron loading process and forwarding toward Complex IV of the mtETC.…”

“…Most abiotic stresses lead to increased ROS production (Sharma et al 2012 ; Das and Roychoudhury 2014 ), but only some of them have been tested to evaluate if their action leads to increased production of MG (Nahar et al 2015 ; Melvin et al 2017 ; Gupta et al 2018 ). Previously, we have shown that ammonium stress leads to an imbalance in the oxidation–reduction status of leaf cells, resulting in increased ROS production (Podgórska et al 2013 , 2018a , b ). Moreover, we have reported that in Arabidopsis ammonium nutrition leads to enhancing of the glycolytic pathway that promotes MG production (Borysiuk et al 2018 ).…”

Editorial for Special Issue “Plant Mitochondria”

“…In this Special Issue, “Plant Mitochondria”, a total of 19 articles were accepted with 15 original research articles and 4 review articles broadly covering the field of plant mitochondrial research (Table 1). Manuscripts focused on protein synthesis and degradation [3,4,5,6], abiotic stress [7,8,9,10], OxPhos [11,12,13,14], protein import [15,16,17], ROS and antioxidants [18], and CMS [19,20].…”

“…Galega Vulgar (European olive). Podgórska et al [12] examined the Complex 1 mutant fro1 ( frostbite 1 ) that has a point mutation in the 8 kDa Fe-S subunit NDUFS4 grown on different nitrogen sources. When these plants were grown on NO 3 - they showed a carbon flux towards nitrogen assimilation and energy production, whereas cellulose integration into the cell wall was restricted.…”