Arabidopsis Roots and Shoots Show Distinct Temporal Adaptation Patterns toward Nitrogen Starvation  

Abstract

Nitrogen (N) is an essential macronutrient for plants. N levels in soil vary widely, and plants have developed strategies to cope with N deficiency. However, the regulation of these adaptive responses and the coordinating signals that underlie them are still poorly understood. The aim of this study was to characterize N starvation in adult Arabidopsis (Arabidopsis thaliana) plants in a spatiotemporal manner by an integrative, multilevel global approach analyzing growth, metabolites, enzyme activities, and transcript levels. We determined that the remobilization of N and carbon compounds to the growing roots occurred long before the internal N stores became depleted. A global metabolite analysis by gas chromatography-mass spectrometry revealed organ-specific differences in the metabolic adaptation to complete N starvation, for example, for several tricarboxylic acid cycle intermediates, but also for carbohydrates, secondary products, and phosphate. The activities of central N metabolism enzymes and the capacity for nitrate uptake adapted to N starvation by favoring N remobilization and by increasing the high-affinity nitrate uptake capacity after long-term starvation. Changes in the transcriptome confirmed earlier studies and added a new dimension by revealing specific spatiotemporal patterns and several unknown N starvation-regulated genes, including new predicted small RNA genes. No global correlation between metabolites, enzyme activities, and transcripts was evident. However, this multilevel spatiotemporal global study revealed numerous new patterns of adaptation mechanisms to N starvation. In the context of a sustainable agriculture, this work will give new insight for the production of crops with increased N use efficiency.

Stress-Induced Cytokinin Synthesis Increases Drought Tolerance through the Coordinated Regulation of Carbon and Nitrogen Assimilation in Rice

“…Wild-type plants compensated for the inhibition of NiR by increasing the activity of GDH that mediates the deamination of Glu. Increased GDH deamination activity has been associated with catabolic processes during starvation (Krapp et al, 2011) and during the response of rice plants to salt stress (Nguyen et al, 2005). The increase in GDH deamination activity seen in wild-type plants during water stress would increase the amounts of 2-oxoglutarate, contributing to the maintenance of the TCA cycle and providing ammonia needed for amino acid synthesis (Miyashita and Good, 2008).…”

Maize Source Leaf Adaptation to Nitrogen Deficiency Affects Not Only Nitrogen and Carbon Metabolism But Also Control of Phosphate Homeostasis

“…This allows roots to react fast to changes in the nitrate availability. Addition or removal of nitrate from roots causes almost instant changes in root transport systems (Wang et al, 2003;Krapp et al, 2011). So far, only two high affinity nitrate transporter have been characterized in maize; ZmNRT2.1 seems responsible for nitrate uptake by the epidermis and ZmNRT2.2 for loading of nitrate into the xylem (Trevisan et al, 2008).…”

“…Most of the microarray experiments have been done on plant material deriving from a mixture of different plant parts and tissues; this could complicate the identification of specific responses to N deprivation. The different tasks of specialized plant tissues, such as roots, source leaves, young sink leaves, or senescing leaves, would require very different adaptation strategies to low N (Gifford et al, 2008;Krapp et al, 2011).…”

“…Large-scale microarray analysis of N statusdependent changes is now available from Arabidopsis (Arabidopsis thaliana; Wang et al, 2000Wang et al, , 2003Price et al, 2004;Scheible et al, 2004;Bi et al, 2007;Gutiérrez et al, 2007;Krapp et al, 2011), rice (Oryza sativa; Lian et al, 2006), and maize (Yang et al, 2011). These identified numerous N status-responsive transcripts involved in the nitrate transport and assimilation, the OPP pathway, amino acid metabolism, organic acid metabolism, tetrapyrrole biosynthesis, major carbohydrate, and protein, lipid, and secondary metabolism to changes in the N status of the plant (Wang et al, 2000(Wang et al, , 2003Scheible et al, 2004;Bi et al, 2007;Krapp et al, 2011) but also many genes with unknown roles in adaption to low-N stress. Most of the microarray experiments have been done on plant material deriving from a mixture of different plant parts and tissues; this could complicate the identification of specific responses to N deprivation.…”

Glucose Elevates NITRATE TRANSPORTER2.1 Protein Levels and Nitrate Transport Activity Independently of Its HEXOKINASE1-Mediated Stimulation of NITRATE TRANSPORTER2.1 Expression

“…Nitrate has profound effects on gene expression, hormone synthesis, and plant growth (Krapp et al, 2011;Krouk et al, 2011;Bouguyon et al, 2012) independent of its assimilation, demonstrating that it is sensed and signals cellular responses. Microarray analyses have shown that nitrate levels rapidly influence the expression of many classes of genes involved in their assimilation and metabolism (Wang et al, 2003;Scheible et al, 2004;Bi et al, 2007;Nero et al, 2009).…”