In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant

Abstract

Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron transport chain may improve the energy metabolism of fro1 plants grown on ammonium. Additionally, the observed changes in reactive oxygen species (ROS) metabolism in the apoplast may be important for determining the growth of fro1 under ammonium nutrition. Moreover, bioinformatic analyses showed that the gene expression changes in fro1 plants significantly overlap with the changes previously observed in plants with a modified apoplastic pH. Overall, the results suggest a pronounced connection between the mitochondrial redox system and the apoplastic pH and ROS levels, which may modify cell wall plasticity and influence growth.

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

“…The consequences of limited ability to oxidize cellular oxidants in mutants carrying a point mutation in NDUFS4 (AT5G67590), affecting complex I assembly— frostbite1 [46,47], on plant growth was observed under NH 4 + and NO 3 − (control) nutrition. During NO 3 − assimilation, fro1 plants showed strong growth retardation, compared to WT plants ( Arabidopsis thaliana, ecotype C24) (Figure 1).…”

“…It was shown that fro1 plants had a single point mutation in the nuclear-encoded 18-kDa Fe–S subunit of complex I, which concerned a G-to-A change at an intron–exon junction at the start codon resulting in missplicing and a premature stop codon [46]. Consequently, the lack of NDUFS4 led to the disassembly of complex I [47]. Moreover, the fro1 mutation reduced the expression of stress-inducible genes during chilling conditions, which impaired cold acclimation, whereby mutants also became sensitive to other stress factors like NaCl and osmotic stress [46].…”

“…Moreover, the fro1 mutation reduced the expression of stress-inducible genes during chilling conditions, which impaired cold acclimation, whereby mutants also became sensitive to other stress factors like NaCl and osmotic stress [46]. In contrast to these responses, in our recent study, fro1 plants showed improved resistance to ammonium nutrition [47]. …”

“…Furthermore, use of the fro1 mutant revealed that the combined effect of an impairment of complex I and NH 4 + treatment not only affects mitochondrial functioning in plants, but also changes their extracellular metabolism [47]. It is known that higher cell wall stiffness in response to NH 4 + nutrition, resulting from altered cell wall modifying enzyme activities, can restrict expansion growth of plant cells [58].…”

Changes in the OXPHOS system in leaf and root mitochondria of Arabidopsis thaliana subjected to long-term sulphur deficiency

“…4a, c, d). Tobacco CMSII and A. thaliana frostbite1 mitochondrial mutants that lack Complex I, and cucumber MSC16 mutant with lower level of Complex I, display the compensation of Complex I by additional type II NAD(P)H dehydrogenases (Juszczuk et al 2007;Garmier et al 2008;Juszczuk and Rychter 2009;Podgórska et al 2015). The increased capacity of ND in/ex NADH in root mitochondria of S-deficient bean and A. thaliana and in Fe-deficient cucumber may be responsible for rapid adjustment of respiration during prolonged macro-or micronutrient deficiency (Vigani and Zocchi 2010;Juszczuk and Ostaszewska 2011;Ostaszewska et al 2014).…”