The influence of N metabolism and organic acid synthesis on the natural abundance of isotopes of carbon in plants

Abstract

SUMMARY This paper relates the 13C/12C ratio of C3 plant material relative to that of source CO2 to the N source for growth, the organic N content of the plant, and the extent of organic acid synthesis. The 13C/12C ratio is quantified as Δ, defined as (δ13C substrate –δ13C product)/(1+δ13C product), where δ13C values of substrate or product (i.e. the samples) are defined as [13C/12C]sample]/[(13C/12C)standard]−1. The computation is performed by relating differences in plant composition as a function of N nutrition and acid synthesis to the fraction of plant C which is acquired via Rubisco and via other carboxylases. The fractional contribution of the different carboxylases to C gain is then related, using the known isotopic fractionations exhibited by these carboxylases, in a model to predict the final Δ of the plant (relative to atmospheric CO2). Application of this approach to a ‘typical’ C3 land plant yields predictions of the decrease of Δ relative to a hypothetical case in which all C is fixed via Rubisco. The predicted decreases range from 0–24 %, for NH4+ assimilation (which always occurs in the roots) to 2–80%, for NO3− assimilation in shoots with the organic acid salt which results from acid‐base balance, plus any additional organic acid salts plus free acids for a plant with a basal C:N molar ratio in organic material of 15. Intermediate values are predicted for symbiotic growth with N2, or where NO3− assimilation in root or shoot is accompanied by some acid‐base regulation via OH‐ loss to the root medium. Comparison with published data on the difference in Δ of Ricinus communis cultured with NH4+ or NO3− shows that the measured influence of nitrogen source is in the right direction (NO3− grown plants with a smaller Δ, i.e. a larger deviation from the value predicted for the absence of non‐Rubisco carboxylations) to be explained by the observed difference in composition and hence fractional C contribution by the various carboxylases. However, the effect of N source on Δ is greater than that predicted by the model, i.e. a 2.1 % decrease as opposed to a 0.10 % decrease. It is likely that the major cause of the difference in δ13C of the plants grown on the two N sources is a change in the ratio of transport and biochemical conductances of leaf photosynthesis. Such a change is quantitatively consistent with the lower water use efficiency of NH4+ ‐grown plants. The predicted, and observed, changes in Δ as a function of N source are of the same magnitude as those found for C3 terrestrial species grown at different temperatures or photon flux densities, or in environments yielding different water use efficiencies by changing root water supply relative to shoot evaporation potential. Variations in N source should be added to the factors which might alter δ of plants growing in the field.

Effects of simulated nitrogen deposition and a stable isotopic assessment for the neotropical epiphytic orchid Laelia speciosa

“…This also causes an increase and later reduction in carbon content for plants subjected to increasing doses of nitrogen, as was observed here for Laelia speciosa. However, δ 13 C of Laelia speciosa, which was typical of CAM plants, did not change under the different N doses utilized, contrasting with δ 13 C measured for C 3 plants subjected to supplementary nitrogen (Raven and Farquhar, 1990;Magalhaes et al, 1992).…”

Variations of the natural abundances of nitrogen and carbon isotopes in Triticum aestivum, with special reference to phloem and xylem exudates

“…The data are not inconsistent with the biochemically-based model of Raven & Farquhar (1990) and the data of Richter et al (1995). However, further analysis of the determinants of xylem sap '^C requires inter alia estimation of ^'^C of respired COj from roots and rooting medium which contribute to the C in organic and amino acids via anaplerotic carboxylations, and analysis of the (5^^C of different components of xylem sap.…”

“…Differences in whole-plant S^^C as a function of the site of combined N assimilation can be predicted from the calculations by Raven & Farquhar (1990). Root reduction and assimilation of NO3~-N (or NH^^-N assimilation) involves anaplerotic HCOg" fixation by phosphoenolpyruvate carboxylase (PEPC) in supplying C skeletons for N assimilation and transport to the shoot.…”

“…produced in the leaves by HCO3 -derived from atmospheric CO^ (f. -8%^). Thus, root assimilation of N is predicted to yield 'lighter' (more negative) plant S^'^C than does shoot assimilation, especially if acid-base regulation gives a higher shoot content of organic anions derived from PEPC activity when shoot assimilation of NO^'-N occurs than when N is assimilated in roots (Raven & Farquhar, 1990). Shoot NOg'-N assimilation will also tend to give shoots a more positive (5"C than roots, because shoots contain a greater per unit dry mass of organic N and organic acid anions derived from PEPC activity fixing atmospheric CO.^.…”

AFestschriftin honour of Professor John A. Raven

“…One example is carbon uptake and assimilation (Raven 1970(Raven , 1997Beardall and Raven 1981;Raven and Farquhar 1990;Giordano et al 2005). Raven (1970) argued that photosynthesis in some algae and other aquatic plants involved accumulation of CO 2 analogous to that in C 4 plants rather than reliance on CO 2 diffusion to the carboxylase in vascular plants with C 3 physiology.…”