Elevated CO2 and ammonium nitrogen promoted the plasticity of two maple in great lakes region by adjusting photosynthetic adaptation

Abstract

Introduction: Climate change-related CO₂ increases and different forms of nitrogen deposition are thought to affect the performance of plants, but their interactions have been poorly studied.

Methods: This study investigated the responses of photosynthesis and growth in two invasive maple species, amur maple (Acer ginnala Maxim.) and boxelder maple (Acer negundo L.), to elevated CO₂ (400 µmol mol^-1 (aCO₂) vs. 800 µmol mol^-1 (eCO₂) and different forms of nitrogen fertilization (100% nitrate, 100% ammonium, and an equal mix of the two) with pot experiment under controlled conditions.

Results and discussion: The results showed that eCO₂ significantly promoted photosynthesis, biomass, and stomatal conductance in both species. The biochemical limitation of photosynthesis was switched to RuBP regeneration (related to J_max) under eCO₂ from the Rubisco carboxylation limitation (related to V_cmax) under aCO₂. Both species maximized carbon gain by lower specific leaf area and higher N concentration than control treatment, indicating robust morphological plasticity. Ammonium was not conducive to growth under aCO₂, but it significantly promoted biomass and photosynthesis under eCO₂. When nitrate was the sole nitrogen source, eCO₂ significantly reduced N assimilation and growth. The total leaf N per tree was significantly higher in boxelder maple than in amur maple, while the carbon and nitrogen ratio was significantly lower in boxelder maple than in amur maple, suggesting that boxelder maple leaf litter may be more favorable for faster nutrient cycling. The results suggest that increases in ammonium under future elevated CO₂ will enhance the plasticity and adaptation of the two maple species.

Keywords: amur maple; boxelder maple; global change; nitrogen form; photosynthetic adaptation.

Figure 1

A sample of a photosynthetic light response curve (lrc) with relevant parameters (A) the photosynthetic rate at saturation light and 400 µmol mol⁻¹ CO₂ (A_n-max ), the curvature of the lrc (Theta, θ), apparent quantum yield (the initial slope of lrc, AQY), and light compensation point (LCP). A_n vs. C_i derived from the lrc database (B), where A_n-total and A_n-total/C_a are the y-intercept and slope of the A_n - C_i regression line. From (B), A_n-total /C_a = A_{n-max /}(C_a - C_i ), so A_n-max /A_n-total = (C_a - C_i )/C_a , which means that A_n-max /A_n-total + C_i /C_a = 1.

Figure 2

Biomass responses to CO₂ and N form treatments in amur maple (A) and boxelder maple (B). “a-” means ambient CO₂ (400 µmol mol⁻¹) and “e-” means elevated CO₂ (800 µmol mol⁻¹) treatments. NH4: fertilized 10 mM (NH₄)₂SO₄; NN: fertilized with a combination of 5 mM (NH₄)₂SO₄ and 5 mM NaNO₃; NO3: fertilized with 10 mM NaNO₃. Means (± SE, n=6) with different letters indicated significant differences between treatments (Tukey host hoc test, P<0.05).

Figure 3

Leaf N partitioning into carboxylation (N_cb ), electron transfer (N_et ), light capture systems (N_lc ), and respiratory (N_resp ) in response to CO₂ and different N forms in amur maple (A) and boxelder maple (B). “a-” means ambient CO₂ (400 µmol mol⁻¹) and “e-” means elevated CO₂ (800 µmol mol⁻¹) treatments. NH4: fertilized with 10 mM (NH₄)₂SO₄; NN: fertilized with a combination of 5 mM (NH₄)₂SO₄ and 5 mM NaNO₃; NO3: fertilized with 10 mM NaNO₃.

Figure 4

Effects of CO₂ and N forms on photosynthetic nitrogen use efficiency [PNUE, (A) and photosynthetic rate at growth CO₂ (A_n-g , (B)] in amur maple (am) and boxelder maple (bm). aCO₂: ambient CO₂ (400 µmol mol⁻¹); eCO₂: elevated CO₂ (800 µmol mol⁻¹); NH4: fertilized with 10 mM (NH₄)₂SO₄; NN: fertilized with a combination of 5 mM (NH₄)₂SO₄ and 5 mM NaNO₃; NO3: fertilized with 10 mM NaNO₃. Means (± SE, n=6) with different letters indicated significant differences between treatments (Tukey host hoc test, P<0.05).

Figure 5

The A/Ci curves in response to different N forms in amur maple (am, A–F) and boxelder (bm, G–L) seedlings grown under ambient CO2 (aCO2, A-C in am and G-I in bm) and elevated CO2 (eCO2, D–F in am and J–L in bm). NH4: fertilized with 10 mM (NH4)2SO4 (left column); NN: fertilized with a combination of 5 mM (NH4)2SO4 and 5 mM NaNO3 (middle column); NO3: fertilized with 10 mM NaNO3 (right column). Each point denotes the means of six (C_i , A_n ) values in A/C_i curve. The circles represent the transition point (C_i-t , A_n-t ) from Rubisco carboxylation to RuBP regeneration of photosynthesis limitation. The triangles indicated the photosynthetic rate (C_i-g , A_n-g ) under growth C_a (400 µmol mol⁻¹ versus 800 µmol mol⁻¹). ACE: apparent carboxylation efficiency estimated from the initial slope of A/C_i curve; Γ_ACi : CO₂ compensation point estimated from A/C_i curve intersects point on X-axis. Different letters of the same parameter in the same species are significantly different between treatments (Tukey host hoc test, P<0.05, see Supplementary Table S2 ).

Figure 6

The relative photosynthesis limitations of biochemistry (l_b ), stomatal resistance (l_s ), and mesophyll resistance (l_m ) in response to CO₂ and N form treatment in amur maple (A) and boxelder maple (B). Abbreviations are provided in Supplementary Table S1 .

Figure 7

Principal Component Analysis (PCA) on growth and photosynthetic parameters in amur maple exposed to CO₂ (A) and N resource (B) treatments and in boxelder maple (C, D). The arrows point to near overlap, vertical, and reverse, which represent positive, no, and negative correlations between these parameters respectively. aCO₂: ambient CO₂ (400 µmol mol⁻¹); eCO₂: elevated CO₂ (800 µmol mol⁻¹); NH4: fertilized 10 mM (NH₄)₂SO₄; NN: fertilized 10 mM N from 5 mM (NH₄)₂SO₄ and 5 mM NaNO₃; NO3: fertilized 10 mM NaNO₃. J_max : maximum of photosynthetic electron transport rate; PNUE: photosynthesis nitrogen use efficiency; A_n-t : net photosynthesis rate at transition point (C_i-t , A_n-t ) between Rubisco limitation and RuBP regeneration limitation based on A/C_i curve; A_n-g : net photosynthesis rate at a growth [CO₂] which eCO₂ at 800 µmol mol⁻¹ and aCO₂ at 400 µmol mol⁻¹; g_s : stomatal conductance; N_leaf : total N of the whole-plant leaf; Chl: leaf chlorophyll concentration; C_i /C_a : the ratio of C_i and C_a ; N_area : leaf N per unit area; SLA: specific leaf area; A_n-max /A_n-total : the ratio of photosynthetic rate of saturation light at 400 µmol mol⁻¹ (A_n-max ) and the y-intercept of A_n vs. C_i fitting line (A_n-total ) from light response curve database; A_n-total/C_a : the slope of A_n vs. C_i fitting line from light response curve database; C/N: leaf carbon and nitrogen ratio; V_cmax : maximum rate of ribulose-1,5-bisphosphate carboxylation; See Supplementary Table S1 for other explanations.

Figure 8

The priori (showing all tested paths) piecewise structural equation model (pSEM) relating to direct and indirect effects of CO₂ and N form on biomass (A) and A_n-g(B). Two CO₂ treatments (ambient CO₂: 400 µmol mol⁻¹ and elevated CO₂: 800 µmol mol⁻¹) and N source (10 mM N source by three forms: NH₄ ⁺, NH₄ ⁺+NO₃ ^- in 1:1, NO₃ ^-) are treated as categorical variables. A_n-g : net photosynthesis rate at a growth [CO₂] which eCO₂ at 800 µmol mol⁻¹ and aCO₂ at 400 µmol mol⁻¹; N_area : leaf N per unit area; SLA: specific leaf area; Chl: leaf chlorophyll concentration; g_t : total conductance to CO₂ between the leaf surface and carboxylation sites (1/_gt = 1/g_s + 1/g_m ). Multiple regression from V_cmax and J_max to A_n-g was used to construct photosynthetic capacity as a component variable (hexagonal frame). The SEM (using psem function in piecewiseSEM package R) of biomass and A_n-g in amur maple are in (C, D), while that of boxelder maple are in (E, F). Arrows mean the directional influence between the variables and the solid lines represent significant relationships, and the dashed lines refer to nonsignificant relationships (P > 0.05). The numbers on top of the arrows represent the standardized path coefficients (for continuous variables), and the numbers under the box with R² refer to the degree of variation of the variable interpreted by all paths. Curved double arrows represent a significant correlation between variables (with correlation coefficient). The values on the line from the categorical variable indicated the continuous variable estimated marginal means by the treatment levels.