Plant delta 15N correlates with the transpiration efficiency of nitrogen acquisition in tropical trees

Abstract

Based upon considerations of a theoretical model of (15)N/(14)N fractionation during steady-state nitrate uptake from soil, we hypothesized that, for plants grown in a common soil environment, whole-plant delta(15)N (deltaP) should vary as a function of the transpiration efficiency of nitrogen acquisition (F(N)/v) and the difference between deltaP and root delta(15)N (deltaP - deltaR). We tested these hypotheses with measurements of several tropical tree and liana species. Consistent with theoretical expectations, both F(N)/v and deltaP - deltaR were significant sources of variation in deltaP, and the relationship between deltaP and F(N)/v differed between non-N(2)-fixing and N(2)-fixing species. We interpret the correlation between deltaP and F(N)/v as resulting from variation in mineral nitrogen efflux-to-influx ratios across plasma membranes of root cells. These results provide a simple explanation of variation in delta(15)N of terrestrial plants and have implications for understanding nitrogen cycling in ecosystems.

Figure 1.

A simplified model of steady-state nitrate uptake, based on the conceptual model of Comstock (2001). F_In is the influx of nitrate from the soil solution into root cells; F_En is the efflux of nitrate from root cells back to the soil solution; F_Rn is the assimilation flux of nitrate into organic molecules within root cells; and F_Xn is the flux of nitrate from root cells into the xylem. Nitrate loaded into the xylem is carried to the leaf in the transpiration stream, where it can also be assimilated into organic molecules. Because nitrate is not exported from leaves in the phloem, the flux of nitrate into the xylem in the root is equal to the assimilation flux in the shoot in the steady state. The discrimination against ¹⁵N during nitrate reduction in both the root and the shoot is defined as b, which is a constant. F_In, F_En, and F_Xn are assumed to proceed without discrimination against ¹⁵N.

Figure 2.

δ_P plotted against F_N/v (A) and δ_P − δ_R (B). Dashed lines represent least-squares linear regressions. Regression equations and statistics are given in each panel. The regression analysis in A does not include the leguminous tree species P. pinnatum, represented by black hexagons, which are enclosed in gray circles to make them more discernible. This species forms N₂-fixing nodules on its roots, which is expected to alter δ_P through an additional process not present in the other species. White symbols with internal cross-hairs refer to conifer tree species; completely white symbols refer to angiosperm liana species; black symbols and black symbols with internal cross-hairs refer to angiosperm tree species.

Figure 3.

A, δ_P plotted against δ_P − δ_R for five individuals each of two angiosperm tree species, T. grandis and S. macrophylla. B, Variation between the two species in F_N/v of the same plants. Dashed lines in A are least-squares linear regressions. Error bars in B represent 1 sd.

Figure 4.

A sensitivity analysis of the predicted relationship between whole-plant δ¹⁵N and F_N/v as a function of the proportion of nitrogen uptake from the soil as nitrate versus ammonium (A), the proportion of nitrate assimilation in roots versus leaves (B), and the δ¹⁵N difference between soil nitrate and soil ammonium (C). Equation 17 was used to predict whole-plant δ¹⁵N, assuming no fixation of atmospheric N₂ and no uptake of organic nitrogen from the soil (i.e. F_Nd = 0, F_No = 0). Ratios of net flux to influx for soil nitrate and ammonium were assumed to correlate linearly with the transpiration efficiency of nitrogen acquisition for each nitrogen source, according to the following relationships: (F_Nn/F_In) = (F_Nn/v)/100 and (F_Na/F_Ia) = (F_Na/v)/100. The range of parameter values considered for each analysis is given above each panel. If a parameter value is not given above the panel, the following were assumed: (F_Nn/F_N) = 0.5, (F_Na/F_N) = 0.5, b = 15‰, c = 17‰, (F_Rn/F_Nn) = 0.5, δ_Sn = 3‰, and δ_Sa = 7‰.

Figure 5.

δ_P plotted against F_N/v for seven tropical tree species. White symbols refer to leguminous tree species capable of forming N₂-fixing nodules on their roots, and black symbols refer to tree species incapable of N₂ fixation. The solid line and the dashed line represent least-squares linear regressions for non-N₂-fixing species and N₂-fixing species, respectively. Data presented in this figure were originally published by Cernusak et al. (2007a).