Nutrient uptake and allocation at steady-state nutrition

Ingestad, T. and Ågren, G. I. 1988. Nutrient uptake and allocation at steady-state nutrition. - Physiol. Plant. 72: 450–459. Net nutrient uptake and translocation rates are discussed for conditions of steady-state nutrition and growth. Under these conditions, the relative uptake rate is equal to the relative growth rate, for whole plants as well as for plant parts, since the root/shoot ratio and internal concentrations remain stable. The nutrient productivity and the minimum internal concentration are parameters characteristic for the plant and the nutrient. A conceptual, mathematical model, based on these two fundamental parameters is used for calculation and prediction of the net nutrient uptake rate, which is required to maintain steady-state nutrition at a specified internal nutrient concentration or relative growth rate. When uptake rate is expressed on the basis of the root growth rate, there is, up to optimum, a strong linear relationship between uptake rate and the internal concentration of the limiting nutrient. More complicated and less consistent relationships are obtained when uptake rate is related to root biomass. The limiting factor for suboptimum uptake is the amount of nutrients becoming available at the root surface. When replenishment is efficient, e.g. with vigorous stirring, the concentration requirement at the root surface appears to be extremely low, even at optimum. In the suboptimum range of nutrition, the effect of nutrient status on root growth rate is a critical factor with a strong feed-back on nutrition, growth and allocation. At supraoptimum conditions, the uptake mechanism is interpreted as a protection against too high uptake rates and internal concentrations at high external concentration. In birch (Betula pendula Roth.), the allocation of nitrogen to the shoots is high compared to that of potassium and also to that of phosphorus at low nitrogen or phosphorus status. With decreasing stress, phosphorus allocation becomes more and more similar to nitrogen allocation. The formulation of a mathematical model for calculation of allocation of biomass and nutrients requires more exact information on the quantitative dependence of the growth-regulating processes on nutrition.     

Theories and methods on plant nutrition and growth

A theory comprising two basic concepts relating nutrition and growth is presented. The first concept is a nutrient flux model and is based upon studies of plants at constant internal nutrient concentrations, where a formal mathematical derivation shows that the relative uptake rate (R_U) and the relative growth rate (R_G) are equal. Deviations from equality are results of experimental insufficiencies and errors. The second concept is based on the observation that R_G is linearly related to the internal nutrient concentration. The slope represents nutrient productivity (P_n), an important parameter expressing growth rate per unit of nutrient. Light and the plant genome, for example, influence the value of the proportionality factor, P_n, but not the formal relationship between the internal nutrient concentration and R_G Not only the theory itself but many results and conclusions are very different from those obtained with traditional methods. In experiments where R_U was controlled during the exponential period of growth, the relationships between treatment (the relative addition rate, R_A), nutrient uptake (R_U) and growth (R_G) were reproduced with extremely low variability. In agreement with theory, internal nutrient concentration and R_G remained stable over time (steady-state). An extension of the theory is based upon the empirical assumption that after exponential growth, self-shading and ageing reduce P_n in proportion to biomass. This assumption has been successfully applied in predicting growth of forest stands, but the nature of the growth reduction is little understood. The generalized model has few parameters and can easily be rewritten to suit different experimental aims, for example to establish reference values and to model changes in soil fertility. Further extension and understanding of the model and different interpretations of the parameters are discussed.     

Nutrition and growth of birch and grey alder seedlings in low conductivity solutions and at varied relative rates of nutrient addition

Birch (Betula verrucosa Ehrh.) and grey alder (Alnus incana Moench) seedlings were grown with varied relative addition rates of all nutrients, up to optimum for vegetative growth. The root medium was basically distilled water to which the nutrients, contained in stock solutions in fixed proportions, were added every second hour and in exponentially increased amounts for consumption during the subsequent period. The nutrient weight proportions previously found to be required in birch (100 N:65 K:13 P) were used in all treatments. However, the nutrient proportions required in grey alder were found to be somewhat different (100 N:50 K:18 P). The use of the required proportions in the additions was important for maintenance of maximum growth, efficient nutrient utilization, and low concentrations in the root medium. Luxury consumption and inefficiency occurred at high concentrations. The results show that the nutrient requirements are sufficiently defined, for different relative growth rates, by the nutrient proportions and the relative addition rate. No clear relationships were found between conductivity or concentration in the root medium and the addition rate, net uptake rate, nutrient status, or relative growth rate. The results are in good agreement with data from low concentration and depletion experiments reported in the literature, showing that non-limited uptake rates occur down to very low concentrations. Thus, there is strong evidence that concentration has been incorrectly used when applied as the treatment variable for plant nutrition in plant science and cultivation practice. The dominant factors in sub-optimum and optimum nutrition are the amounts of nutrients available per unit of time, the growth rate, and the nutrient proportions. At low concentration levels, physical factors such as stirring and flow rate of nutrient solution and boundary layer effects are decisive for the rates with which the nutrients become available to the roots. Therefore, at low levels, concentration alone cannot be used as the factor determining nutrient uptake rate. At high levels, concentration is effective as a supra-optimum factor and increased internal percentage contents cause decreased uptake efficiency, thus counter-acting the concentration effect. Nitrogen effects dominated the stress indications when the internal nitrogen percentage content decreased from optimum to the level of the treatments in the beginning of the experiments. Leaf deficiency symptoms disappeared and the root/shoot ratio change ceased when nitrogen status stabilized. Strong linear regressions were found between any two of the variables: relative addition rate of nutrients, relative growth rate, and nutrient status.     

Dependence of starch storage on nutrient availability and photon flux density in small birch Betula pendula Roth)

Abstract Small birch plants (Betula pendula Roth) were grown in a climate chamber at different levels of nutrient availability and at two photon flux densities. The extent to which starch storage was dependent upon nutrient availability and photon flux density was investigated. Acclimated values of starch concentration in leaves were highest at low nutrient availability and high photon flux density. Starch storage in roots was only found at the lowest nutrient availability. However, the relative rate of starch storage (starch stored per unit plant dry weight and time) was higher in plants with good nutrition. The data suggest that, at sub-optimal nutrient availability, the momentary rate of net shoot photosynthesis is unlikely to limit the structural (as opposed to carbon storage) growth of the plant. Although photosynthetic rate per unit leaf area (as measured at the growth climate) was slightly lower in plants with poor nutrient availability, photosynthetic rate per unit leaf nitrogen was higher. These data suggest a priority of leaf nitrogen usage in photosynthesis, with limiting amounts of leaf nitrogen (and possibly other nutrients) for subsequent growth processes. This argument is consistent with the higher concentrations of starch found in plants with poor nutrient availability.     

Growth, nutrition, and nitrogen fixation in grey alder at varied rate of nitrogen addition

Seedlings of grey alder (Alnus incana Moench), nodulated or unnodulated, were investigated at varied relative addition rate of nitrogen. Nitrogen fixation alone, without addition of mineral nitrogen, resulted in an almost optimum nitrogen status but only about half the maximum relative growth rate, probably mainly because of energy costs of nodulation and fixation. The growth deficit due to nodulation was much more than can be explained by the theoretical energy requirement for the amount of nitrogen fixed. Thus, the nitrogen fixation process was not very efficiently used. The nitrogen fixation rate was strongly stimulated by increasing nitrogen addition rate up to high levels. The fixation rate decreased rapidly close to optimum (maximum relative growth rate) and was negligible at maximum growth. A feed-back of mineral nitrogen on photosynthesis increased fixation rate with time, and the relative importance of fixation over mineral nitrogen nutrition increased. However, nitrogen fixation, also at maximum rate, supplied only a small proportion of the nitrogen amount required for maximum growth. The optimum nutrient solutions contained comparatively high nitrogen concentrations to secure free access to nitrogen. The nodules were damaged by this treatment, and it is concluded that the nitrogen additions must be adjusted to the current consumption of the plants to avoid an increased external nitrogen concentration. Strong linear regressions were found between relative growth rate, nitrogen status expressed as percentage content of fresh weight, and relative growth rate in unnodulated seedlings. There was a greater variability in nodulated seedlings than in unnodulated ones, because of the nitrogen fixation. The reactions of unnodulated grey alder were largely the same as previously reported for birch seedlings, but the maximum growth capacity was lower in grey alder. During an initial period of change in the internal nitrogen status, deficiency symptoms appeared, especially in unnodulated seedlings. As in birch, the leaves turned green again at stable nitrogen status, independent of level. The results are in sharp contrast to data from the literature where the external nitrogen concentration was used as the driving variable for the internal nitrogen status. The measured fixation rates for grey alder are much higher than those previously reported. Still, the maximum fixation rate observed is small compared to the total nitrogen uptake rate required for maximum growth, in contrast to reported relationships. These comparisons indicate that increased external nitrogen concentration obscures the real relations between mineral and fixed nitrogen, on one hand because of rapid inhibition of nitrogen fixation and, on the other hand, because of failure to obtain stable optimum nutrition and maximum growth by means of this treatment variable.     

How do nutrients drive growth?

The relationship between plant nutrient concentration and relative growth rate (RGR) was studied under non-steady state conditions using data from a new N interruption experiment with young lettuce plants grown hydroponically in the glasshouse. RGRs estimated from the fit of a versatile growth model were shown to decline curvilinearly with plant N concentration as N deficiency increased. Similar curvilinear relationships were also derived when the same model was used to reanalyse data for N, P and K interruption treatments from other experiments previously published in the literature. These results clearly indicate that the rate of remobilisation of nutrient reserves varies with the nutrient status of the plant. This contrasts with the linear relationships observed where the changes in plant N concentration occurred solely as a response to increasing plant age, or when plants were grown under steady state conditions with constant relative nutrient addition rates. These differences in the pattern of response provide strong evidence to support the hypothesis that the form of the relationship between RGR and plant nutrient concentration can vary depending upon whether a plant's external supplies or internal reserves of a particular nutrient are more limiting.     

Nutrition and growth of coniferous seedlings at varied relative nitrogen addition rate

The growth of two provenances of Pinus sylvestris L. were compared with two provenances of Picea abies (L.) Karst. and with Pinus contorta Dougl. when grown in solution cultures with low nutrient concentrations. Nitrogen was added at different exponentially increasing rates, and the other nutrients were added at a rate high enough to ensure free access of them to the seedlings. During an initial period of the culture (a lag phase), when the internal nutrient status was changing from optimum to the level of the treatment, deficiency symptoms appeared. The needles yellowed and the root/shoot ratio increased. The initial phase was followed by a period of exponential growth and steady-state nutrition. The needles turned green again, and the root/shoot ratio stabilized at a level characteristic of the treatment. These patterns were the same as previously reported for other tree species. The relative growth rate during exponential growth was numerically closely equal to the relative nitrogen addition rate. The maximum relative growth rates were about 6 to 7.5% dry weight increase day^-1. This is a much lower maximum than for broad-leaved species (about 20 to 30% day^-1) under similar growth conditions. The internal nitrogen concentrations of the seedlings and the relative growth rates were stable during the exponential period. Close linear relationships were found between these parameters and the relative addition rate up to maximum growth. During steady state the relative growth rates of the different plant parts were equal. However, there were large differences between genotypes in absolute root growth rate at the same seedling size because of differences in root/shoot ratio. Lodgepole pine had the highest root growth rate, whereas that of Norway spruce, especially the southern provenance, was remarkably low. Yet, Norway spruce had a high ability to utilize available nutrients. In treatments with free nutrient access, growth allocation to the shoot had a high priority in all genotypes, but there was still a marked tendency for luxury uptake of nutrients. Nitrogen productivity (growth rate per unit of nitrogen) was lower than in broadleaved species and highest in lodgepole pine. The relevance of the dynamic factors, i.e. maximum relative growth rate, nutrient uptake rate, nitrogen productivity, growth allocation and root growth rate, are discussed with regard to conifer characteristics and selection value.     

Interaction between nitrogen and photon flux density in birch seedlings at steady-state nutrition

Birch ( Betula pendula Roth.) was investigated under steady-state nutrition and growth at different incident photon flux densities (PFD) and different relative addition rates of nitrogen. PFD had a strong influence on the relative growth rate at optimum nutrition and on the nitrogen productivity (growth rate per unit of nitrogen) but little effect on the formal relationships between nitrogen and growth, i.e. PFD and nitrogen nutrition are orthogonal growth factors. At a given suboptimum nitrogen (the same distance from optimum), increased PFD increased the relative growth rate and, therefore, the relative uptake rate and the required relative addition rate in accordance with the theoretical equality between these three parameters at steady-state nutrition. Correspondingly, at a given suboptimum relative addition rate, increased PFD decreased nitrogen status (larger distance from optimum) at an unchanged relative growth rate. Nutrient uptake rate, dry matter content, and partitioning of biomass and nutrients are strongly influenced by nitrogen status. PFD influences these characteristics, but only to an extent corresponding to its effect on the nitrogen status. The influence of PDF on the relative growth rate at optimum and on nitrogen productivity is well described by hyperbolic relationships, similar to reported PFD/photosynthesis relationships. These expressions for plant growth as well as the productivities of leaf area and quantum appear to be valuable characteristics of plant responses to light and nutrition. Although the calculated PFD/growth relationships indicate saturation at high values of PFD, a more realistic estimate of PFD at which saturation occurs is about 30 mol m⁻² day⁻¹, where the highest relative growth rate and nitrogen productivity were experimentally determined. No significant effect was observed because of day length differences between the present and previous experiments.     

Nutrition and growth of birch seedlings at varied relative phosphorus addition rates

Birch ( Betula pendula Roth.) was investigated under steady state nutrition and growth at different relative addition rates of phosphorus (R_p). Phosphorus deficiency symptoms appeared on the leaves when the internal phosphorus concentration decreased, but disappeared again under steady state nutrition, independent of the stress level. The increased root/shoot ratio and the exploratory type of root systems developed during the adjustment stage remained under steady state conditions. At nonoptimum and close to optimum relative addition rates, independent of the rate, the phosphorus concentration of the culture solution did not exceed 2 μmol dm⁻³ and was generally < 1 μmol dm⁻³ immediately after phosphorus additions. The phosphorus concentration just before additions was generally < 0.5 μmol dm⁻³. The nutrition/growth relationships were similar to those for nitrogen, with relative growth rate (R_g) closely related to the R_p applied and with a strong linear relationship between internal phosphorus concentration and R_g. Regression was much steeper than that for nitrogen. The slope of the optimum nutrition was attained at a lower phosphorus weight proportion to nitrogen (8–10 P: 100 N) than previously estimated (= 13 P: 100 N), but a higher relative phosphorus requirement was observed under stress conditions. Birch seedlings had a strong tendency to consume phosphorus in excess of immediate requirements with a small effect on growth above optimum. This resulted in rapidly decreasing phosphorus productivity (P_p, growth rate per unit of phosphorus) with increasing internal phosphorus concentrations above optimum.     

A theoretical explanation of the Piper-Steenbjerg effect

The relation between plant yield and plant nutrient concentration is sometimes found to be negative, a phenomenon called the Piper-Steenbjerg (PS) effect. A model was used to examine the underlying causes of the PS effect, and the conditions under which it is most likely to occur. The model uses the nutrient productivity concept for plant growth and a nutrient uptake equation in which root growth rate and external nutrient concentration determine the uptake rate. The study suggests that the PS effect occurs when the fast growth of plants grown in an initially higher nutrient medium eventually leads to a more rapid depletion of external nutrients than the slow growth of plants grown in an initially lower nutrient medium. The fast growth of plants combined with a rapid decrease of nutrient uptake leads to a fall in plant nutrient concentration. When these large plants with very low nutrient concentrations are compared with the smaller, slow-growing plants, a PS effect may be found depending on the time at which the plants are harvested, and on the range of initial values of the external nutrient content. When it occurs, the effect is greatest when the depletion volume per unit new root (V_d) is lowest, and when the mobility of nutrients in the medium is highest (α=1). The results are sufficiently general to apply to a variety of nutrients, plant species and growth media.