Mitochondrial uncoupling protein contributes to the regulation of carbon and nitrogen metabolism and seed yield under low nitrogen stress in Arabidopsis

Abstract

Nitrogen (N) availability is a critical factor for plant development and yield, and it closely correlates to carbon (C) metabolism. Uncoupling protein (UCP) and alternative oxidase (AOX) in mitochondria exhibit a strong correlation with N and C metabolism. Here, we investigated the respective functions of UCP and AOX by using ucp1, aox1a and aox1a/ucp1 mutants under low-N condition. Low-N markedly increased AOX1a and UCP1 expression, alternative pathway capacity and UCP activity. Eight-day-old aox1a/ucp1 seedlings were more sensitive to low-N condition than Col-0 and single mutants, i.e., the lower primary root length and higher anthocyanin accumulation. The net photosynthetic rate (A) and electron transport rate (ETR) under low-N stress were markedly decreased in ucp1 and aox1a/ucp1 compared to those in Col-0, but not in aox1a. The leaf area, total C and N content in shoots showed a similar profile as A and ETR. Nitrate acquisition rate was accelerated in aox1a/ucp1, but its transport activity from root to shoot was decreased, which resulted in the low nitrate content and nitrate reductase activity in shoots upon low-N condition. Additionally, the low C and N content in ucp1 and aox1a/ucp1 seeds led to the decreased seed yield compared to Col-0 upon low-N stress. RNA-seq analysis revealed that a large number of genes involved in photosynthesis, C/N metabolism were markedly down-regulated in aox1a/ucp1 compared to Col-0 under low-N stress. These results highlight the more key role of UCP1 than AOX1a in modulating C and N metabolism and seed yield in Arabidopsis adaptation to low-N stress.