Dynamics of leaf and root growth: endogenous control versus environmental impact

Abstract

Aims: Production of biomass and yield in natural and agronomic conditions depend on the endogenous growth capacity of plants and on the environmental conditions constraining it. Sink growth drives the competition for carbon, nutrients and water within the plant, and determines the structure of leaves and roots that supply resources to the plant later on. For their outstanding importance, analyses of internal growth mechanisms and of environmental impact on plant growth are long-standing topics in plant sciences.

Scope: Recent technological developments have made it feasible to study the dynamics of plant growth in temporal and spatial scales that are relevant to link macroscopic growth with molecular control. These developments provided first insights into the truly dynamic interaction between environment and endogenous control of plant growth.

Conclusions: Evidence is presented in this paper that the relative importance of endogenous control versus the impact of the dynamics of the environment depends on the frequency pattern of the environmental conditions to which the tissue is exposed. It can further be speculated that this is not only relevant within individual plants (hence leaves versus roots), but also crucial for the adaptation of plant species to the various dynamics of their environments. The following are discussed: mechanisms linking growth and concentrations of primary metabolites, and differences and homologies between spatial and temporal patterns of root and leaf growth with metabolite patterns.

Fig. 1.

Spatio-temporal patterns of leaf growth in Nicotiana tabacum. (A) Instantaneous, colour-coded distributions of relative elemental growth rates at five different times throughout the diurnal course (night 2000–0800 h). (B) Sequence of instantaneous, colour-coded distributions of relative elemental growth rates (REGR) in response to a day–night transition. (C) Set-up for leaf-growth monitoring and original image. (D) Spatio-temporal distribution of relative elemental growth rates along the midvein (averaged over 2 h and 15 % midvein length). (E) Average relative growth rate (RGR) of the leaf depicted in (B) during the first hour of the night.

Fig. 2.

Spatio-temporal patterns of root growth in Nicotiana tabacum. (A) Set-up for root growth monitoring. (B) Original image and colour-coded distribution of relative elemental growth rates. (C) Instantaneous distributions of relative elemental growth rates at five different times throughout the diurnal course (night 2000–0800 h). (D) Growth velocity of the root tip (V_tip) during four typical diurnal courses (1-h mean values and variations).

Fig. 3.

Growth of isolated leaf discs, cut from growing leaves of Nicotiana tabacum. (A) Relative growth rate (RGR) of a leaf disc floating on nutrient solution in continuous light (LL), 24 h after cutting the disc from a plant that was adapted to 12 h/12 h light/dark (entrained night phase shown in panel). (B) Visualization of leaf disc growth within 4 d. Discs in left Petri dish were cut immediately prior to taking the picture, while disc in the right Petri dish was cut with the same cork borer 4 d earlier. (C) Growth of leaf discs (n = 6, mean value and standard error) in area, fresh and dry weight 5 d after incubation (12 h/12 h light/dark). The leaf discs were all cut with the same borer (17.5-mm diameter) and were incubated either on nutrient solution or double-distilled water. (D) Growth of a leaf disc and of the leaf from which the disc was cut initially. Four days after cutting, the leaf disc, which had floated on nutrient solution, was put back in the hole of the leaf. The leaf was attached to the intact plant for the entire time. The small leaf disc to the right is cut from another leaf and depicts the size of the incubated leaf disc at the time of cutting. Due to the convex shape of the incubated leaf disc, disc and hole do not match perfectly.

Fig. 4.

Metabolite concentrations in growing and mature leaves of Nicotiana tabacum. (A) Time series of starch, sucrose (Suc), citrate and glutamine (Gln) in young, intermediate and full-grown leaves of Nicotiana tabacum throughout the diurnal course. For Suc, citrate and Gln, three leaves of different positions within the same plant were chosen for taking the samples of each point in time. For the young and full-grown leaf, two leaf discs were pooled for the sample. For the intermediate leaf, mean value and standard error of four separately analysed samples are depicted. The eight plants used for this experiment were taken from a total population of 24 plants and were selected for comparable growth rates of the three leaf developmental states investigated: intermediate leaves (RGR = 45 ± 5 % d⁻¹); young leaves, three positions above (RGR = 90 ± 10 % d⁻¹; full-grown leaves, three positions below intermediate leaves (RGR = 0 % d⁻¹). For starch, the samples were taken from intermediate leaves of another population of plants. (B) Spatial distribution of glucose (Glc), fructose (Fru), sucrose (Suc), starch and total amino acids (Tot AA) throughout the leaf blade in inter-veinal tissue of intermediate leaves of Nicotiana tabacum. Samples were taken at the indicated positions along the leaf developmental axes in parallel to the midvein and the side veins of first order (n = 6, mean value and standard error). The six plants used for this experiment were taken from a total population of 24 plants and were selected for comparable growth rates of intermediate leaves (RGR = 45 ± 2 % d⁻¹). (C) Ratio of glucose/fructose (Glc/Fru) along the leaf midvein, calculated from the values depicted in (B) (mean values and standard error).