Carbon and nitrogen nutrient balance signaling in plants

Abstract

Cellular carbon (C) and nitrogen (N) metabolism must be tightly coordinated to sustain optimal growth and development for plants and other cellular organisms. Furthermore, C/N balance is also critical for the ecosystem response to elevated atmospheric CO(2). Despite numerous physiological and molecular studies in C/N balance or ratio response, very few genes have been shown to play important roles in C/N balance signaling. During recent five years, exciting progress was made through genetic and genomic studies. Several DNA microarray studies have shown that more than half of the transcriptome is regulated by C, N and the C-N combination. Three genetic studies involving distinct bioassays have demonstrated that a putative nitrate transporter (NTR2.1), a putative glutamate receptor (GLR1.1) and a putative methyltransferase (OSU1) have important functions in the C/N balance response. OSU1 is identical to QUA2/TSD2 which has been implicated to act in cell wall biogenesis, indicating a link between cell wall property and the C/N balance signaling. Given that many investigations are only focused on C alone or N alone, the C/N balance bioassays and gene expression patterns are discussed to assist phenotypic characterization of C/N balance signaling. Further, re-examination of those previously reported sugar or nitrogen responsive genes in C/N balance response may be necessary to dissect the C/N signaling pathways. In addition, key components involved in C-N interactions in bacterial, yeast and animal systems and whether they are functionally conserved in plants are discussed. These rapid advances have provided the first important step towards the construction of the complex yet elegant C/N balance signaling networks in plants.

Figure 1

A simplified whole plant view of tightly coordinated C and N metabolism. C assimilation and N uptake occur in the leaf and the root systems, respectively. 2-oxoglutarate (2OG), an important intermediate product of C metabolism, serves as the C-skeleton for the synthesis of glutamate (which uses photorespiratory ammonium; not drawn here). Ammonium (NH₄⁺) resulted from primary N assimilation from nitrate (NO₃⁻) is then incorporated to glutamate, and glutamine is synthesized. Other amino acids are then synthesized by using NH₄⁺ donated from glutamate and glutamine, and therefore proteins can be synthesized. Proteins are essential for almost all of cellular activities, including C and N metabolism.

Figure 2

C/N balance bioassays and gene expression patterns. (A) An example of osu1–2 hypersensitivity to high C/low N in anthocyanin accumulation. (B) An example of osu1–2 hypersensitivity of root growth inhibition in response to high C/low N and low C/high N. (C) Example of gene expression patterns in response to various C/N ratios. Relative mRNA levels of MYB75 and ASN1 genes, using ACTIN2 as an internal control, are shown. WT, wild-type. C (Suc) and N (total N) are in minimolar concentrations. Note that (A–C) were redrawn using the data published elsewhere. For more details, please see ref. . (D) A proposed mathematical model for C/N balance bioassay and gene expression analysis. Solid lines indicate the four C/N conditions which are recommended the minimum for showing the C/N balance response phenotype, while the dotted lines include other C/N set-ups which will convincingly demonstrate the C/N balance phenotype at various C or N levels or C/N ratios.

Figure 3

Hypocotyl phenotypes of osu1–3 under various C/N conditions. Shown are the representative hypocotyls (right below the hypocotyl-cotyledon junction) from the seven-day-old wild-type (WT) and osu1–3 seedlings grown under four different C/N conditions.