Distinct Carbon and Nitrogen Metabolism of Two Contrasting Poplar Species in Response to Different N Supply Levels

Abstract

Poplars have evolved various strategies to optimize acclimation responses to environmental conditions. However, how poplars balance growth and nitrogen deficiency remains to be elucidated. In the present study, changes in root development, carbon and nitrogen physiology, and the transcript abundance of associated genes were investigated in slow-growing Populus simonii (Ps) and fast-growing Populus euramericana (Pe) saplings treated with low, medium, and high nitrogen supply. The slow-growing Ps showed a flourishing system, higher δ¹⁵N, accelerated C export, lower N uptake and assimilation, and less sensitive transcriptional regulation in response to low N supply. The slow-growing Ps also had greater resistance to N deficiency due to the transport of photosynthate to the roots and the stimulation of root development, which allows survival. To support its rapid metabolism and growth, compared with the slow-growing Ps, the fast-growing Pe showed greater root development, C/N uptake and assimilation capacity, and more responsive transcriptional regulation with greater N supply. These data suggest that poplars can differentially manage C/N metabolism and photosynthate allocation under different N supply conditions.

Keywords: net inorganic nitrogen flux; nitrogen uptake; photosynthate allocation; stable nitrogen isotope; transcriptional regulation.

Figure 1

A schematic model of C/N metabolism in plants. Glyceraldehyde 3-phosphate (G3P) produced by CO₂ fixation in Calvin cycle can be exported to the cytosol or used to synthesize starch in chloroplast. Sucrose is synthesized by the enzyme sucrose phosphate synthase (SPS) via the consumption of uridine diphosphate glucose (UDP-G) from the Calvin cycle and fructose-6-phosphate. Sucrose can be transported to the sink tissues and hydrolyzed to glucose and fructose by cell wall invertase (CWI) and vacuolar invertase (VI). The glucose is phosphorylated by hexokinases (HxKs) and further utilized for glycolysis and respiration. NH₄⁺ and NO₃⁻ are absorbed in the roots by various transporters for ammonium (AMTs) and nitrate (NRTs). After uptake, NO₃⁻ is reduced to NH₄⁺ via nitrate reductase (NR) and nitrite reductase (NiR). Then, NH₄⁺ is assimilated to glutamine (Gln) and glutamate (Glu) by glutamine synthetase and glutamate synthase (GS/GOGAT) or the glutamate dehydrogenase (GDH) pathways.

Figure 2

Contents of sucrose (A,D), fructose (B,E) and glucose (C,F) of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. * p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant.

Figure 3

Sucrose phosphate synthase (A,D), sucrose synthase (B,E), and hexokinase (C,F) activities of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. * p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant.

Figure 4

Net NH₄⁺ (A), NO₃⁻ (B) and H⁺ (C) fluxes of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1 and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. ** p < 0.01; *** p < 0.001; ns, not significant.

Figure 5

NH₄⁺ (A,D), NO₃⁻ (B,E), and NO₂⁻ (C,F) concentrations of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. ** p < 0.01; *** p < 0.001; ns, not significant.

Figure 6

Total N concentrations (A,C) and δ¹⁵N (B,D) of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. * p < 0.05; *** p < 0.001; ns, not significant.

Figure 7

NR (A,C) and NiR (B,D) activities of P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. Bars labelled with different letters indicate significant difference between the treatments. p-Values of the ANOVAs of species, N treatment, and their interaction are indicated. * p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant.

Figure 8

Principal component analysis (PCA) plot of the first two principal components in P. simonii (Ps) and Populus euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. The analysis was conducted using data of physiological parameters of Ps (circle) and Pe (triangle).

Figure 9

Cluster analysis of transcriptional fold-changes of key genes involved in N uptake and assimilation in roots (A) and leaves (B) of P. simonii (Ps) and P. euramericana (Pe) under 0.01, 1, and 10 mM NH₄NO₃. The colour scale indicates fold-changes of mRNAs. For each gene, the expression levels in roots or leaves of Pp exposed to 1 mM NH₄NO₃ were defined as 1, and the corresponding fold-changes under 0.01 and 10 mM NH₄NO₃ were calculated.