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 thalianafrostbite1 (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.

Keywords

• cell wall synthesis
• complex I defect
• frostbite1
• mitochondrial mutant
• NDUFS4
• necrosis
• sugar catabolism
• sugar signaling
• programmed cell death
• reactive oxygen species