Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate

Abstract

SummaryThe mitochondrial oxidative phosphorylation system in plants possesses a variety of alternative pathways that decrease respiratory ATP production. These alternative pathways are mediated by three classes of bypass proteins: the type II NAD(P)H dehydrogenases (which circumvent complex I of the electron transport chain), the alternative oxidases (AOXs; which circumvent complexes III and IV) and the uncoupling proteins (which circumvent ATP synthase). We have monitored the expression of all genes encoding respiratory bypass proteins in Arabidopsis thaliana growing with different sources of inorganic nitrogen (N). Resupply of nitrate (NO À 3 ) to N-limited seedling cultures caused a decrease in the transcript abundance of several type II NAD(P)H dehydrogenase and AOX genes, while resupply of ammonium (NH þ 4 ) led to broad increases in expression in the same gene families. Similar results were observed upon switching between nitrate and ammonium in the absence of N stress. Nitrate signalling was found to be mediated primarily by the nitrate ion itself, whereas ammonium regulation was dependent upon assimilation and affected by changes in apoplastic pH. Corresponding alterations in alternative respiratory pathway capacities were apparent in seedlings supplied with either nitrate or ammonium as an N source and in mitochondria purified from the seedlings. Specifically, AOX capacity and protein abundance, as well as calcium-dependent external NADH oxidation, were substantially elevated after growth on ammonium. The increased capacity of respiratory bypass pathways after switching from nitrate to ammonium was correlated to an overall respiratory increase.

An analytical model of non‐photorespiratory CO2 release in the light and dark in leaves of C3 species based on stoichiometric flux balance

“…By consuming reductant that may otherwise increase mitochondrial electron flow independent of ATP demand, one may expect NO3 -assimilation to alleviate reductions in po associated with photoreductant flows. Indeed, Escobar, Geisler & Rasmusson (2006) found that in Arabidopsis thaliana, AOX genes were up-regulated in response to NH4 + nutrition, but down-regulated in response to NO3 -nutrition. Our model predicts that the effect of NH4 + nutrition on P : O ratio, and thus presumably on AOX activity, depends on the ATP : 2e -ratio (pe) in photosynthesis.…”

Alternative oxidase and plant stress tolerance

“…Hence preventing excessive mitochondrial ROS, RNS (reactive nitrogen species, designate NO and other NO-related molecules) production by maintaining carbon pool homeostasis, 19 redox state homeostasis in nitrogen assimilation process. 20,21 and energy state homeostasis during mineral ion uptake.…”

Arabidopsis SIZ1 positively regulates alternative respiratory bypass pathways

“…These pathways are not found in other organisms. Interestingly, reorganization of the respiratory bypass pathway in response to nitrogen sources was recently reported (22).…”

“…SIZ1 is a SP-RING finger protein that has a DNA-binding (22). These results suggest that alternative respiration-related genes encoding type II NAD(P)H dehydrogenase and several alternative oxidases must be downregulated in the siz1 mutant and that AtSIZ1 can act as a regulator of an alternative respiratory pathway.…”