Disruption of the mitochondrial alternative oxidase (AOX) and uncoupling protein (UCP) alters rates of foliar nitrate and carbon assimilation inArabidopsis thaliana

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Abstract

We demonstrated that mitochondrial respiration contributes to energy balancing between nitrogen and carbon metabolism by competing for reductant with de novo NO3– assimilation and avoiding chloroplastic excess reductant.

Under high light, the rates of photosynthetic CO2 assimilation can be influenced by reductant consumed by both foliar nitrate assimilation and mitochondrial alternative electron transport (mAET). Additionally, nitrate assimilation is dependent on reductant and carbon skeletons generated from both the chloroplast and mitochondria. However, it remains unclear how nitrate assimilation and mAET coordinate and contribute to photosynthesis. Here, hydroponically grown Arabidopsis thaliana T-DNA insertional mutants for alternative oxidase (AOX1A) and uncoupling protein (UCP1) fed either NO3– or NH4+ were used to determine (i) the response of NO3– uptake and assimilation to the disruption of mAET, and (ii) the interaction of N source (NO3– versus NH4+) and mAET on photosynthetic CO2 assimilation and electron transport. The results showed that foliar NO3– assimilation was enhanced in both aox1a and ucp1 compared with the wild-type, suggesting that foliar NO3– assimilation is probably driven by a decreased capacity of mAET and an increase in reductant within the cytosol. Wild-type plants had also higher rates of net CO2 assimilation (Anet) and quantum yield of PSII (ΦPSII) under NO3– feeding compared with NH4+ feeding. Additionally, under NO3– feeding, Anet and ΦPSII were decreased in aox1a and ucp1 compared with the wild type; however, under NH4+ they were not significantly different between genotypes. This indicates that NO3– assimilation and mAET are both important to maintain optimal rates of photosynthesis, probably in regulating reductant accumulation and over-reduction of the chloroplastic electron transport chain. These results highlight the importance of mAET in partitioning energy between foliar nitrogen and carbon assimilation.

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