'And then there were three': highly efficient uptake of potassium by foliar trichomes of epiphytic bromeliads

Abstract

Background and aims: Vascular epiphytes have to acquire nutrients from atmospheric wash out, stem-flow, canopy soils and trapped litter. Physiological studies on the adaptations to nutrient acquisition and plant utilization of nutrients have focused on phosphorus and nitrogen; potassium, as a third highly abundant nutrient element, has received minor attention. In the present study, potassium uptake kinetics by leaves, within-plant distribution and nutrient accumulation were analysed to gain an improved understanding of physiological adaptations to non-terrestrial nutrient supply of plants.

Methods: Radioactively labelled (86)RbCl was used as an analogue to study uptake kinetics of potassium absorbed from tanks of epiphytes, its plant distribution and the correlation between uptake efficiency and abundance of trichomes, functioning as uptake organs of leaves. Potassium in leaves was additionally analysed by atomic absorption spectroscopy to assess plant responses to potassium deficiency.

Key results: Labelled rubidium was taken up from tanks over a wide range of concentrations, 0.01-90 mm, which was achieved by two uptake systems. In four tank epiphytes, the high-affinity transporters had average K(m) values of 41.2 microm, and the low-affinity transporters average K(m) values of 44.8 mm. Further analysis in Vriesea splenriet showed that high-affinity uptake of rubidium was an ATP-dependent process, while low-affinity uptake was mediated by a K(+)-channel. The kinetic properties of both types of transporters are comparable with those of potassium transporters in roots of terrestrial plants. Specific differences in uptake velocities of epiphytes are correlated with the abundance of trichomes on their leaf surfaces. The main sinks for potassium were fully grown leaves. These leaves thus function as internal potassium sources, which allow growth to be maintained during periods of low external potassium availability.

Conclusions: Vascular epiphytes possess effective mechanisms to take up potassium from both highly diluted and highly concentrated solutions, enabling the plant to incorporate this nutrient element quickly and almost quantitatively from tank solutions. A surplus not needed for current metabolism is stored, i.e. plants show luxury consumption.

Fig. 1.

Time course of rubidium depletion from tanks of Vriesea splenriet. Tanks were filled with a mixture of 2·5 × 10⁷ d.p.m. ⁸⁶Rb⁺ and 75 nmol unlabelled RbCl in 1·5 mL Mes-buffer, 1 mm, pH 6·1, containing 1 mm CaCl₂. Tissue recovery was calculated from the label reanalysed in plant tissue. Data are means ± s.d.; n = 4. The regression equation is indicated.

Fig. 2.

Biphasic kinetics of rubidium uptake from tanks of Vriesea splenriet in the presence of 0·01–90 mm substrate. Experimental detail as in Fig. 1 except that different concentrations of unlabelled RbCl were used as indicated in the diagram. Uptake rates were calculated from the decrease of ⁸⁶Rb⁺ radioactivity during the first 1–2 h of uptake. Data are means ± s.d.; n = 4. The regression equations for the low and high concentration ranges are indicated.

Fig. 3.

Inhibition of rubidium uptake from tanks of Vriesea splenriet by carbonyl cyanide m-chlorophenylhydrazone (CCCP) and tetraethylammonium chloride (TEA) at different Rb⁺ concentrations. Uptake rates are expressed as percentage inhibition by CCCP or TEA compared with a control without inhibitors. Tanks were supplied with 2·5 × 10⁷ d.p.m. ⁸⁶Rb⁺ and 1·5 mL Mes-buffer, 1 mm, pH 6·1, containing 1 mm CaCl₂, rubidium chloride as indicated and either 1 mm CCCP or 1 mm TEA. Other experimental details are as described in Fig. 1. Data are means ± s.d.; n = 4. The regression equations for inhibition by TEA and by CCCP are: y=2·87 (1–e^{−1·2×106x}), r²=0·98; y=6·07 (1–e^−0·13x), r²=0·97.

Fig. 4.

Relationship between rubidium uptake and trichome density in different bromeliads. All plants except large plants of Guzmania monostachia and Werauhia sanguinolenta were measured completely submerged in label solution containing 0·5 mm rubidium chloride and 1 × 10⁷ d.p.m. mL^{−1 86}Rb⁺. Trichome densities were averaged by counting basal, middle and distal parts of the upper and lower side of 4–8 leaves. Uptake rates for large plants from Guzmania and Werauhia were measured in the same label solution using discs prepared from basal, middle and distal sections of upper and lower sides of older and younger leaves. Trichome density is given as number per mm⁻². Abbreviations: Vr_L = Vriesea splenriet (plants of the same size as used in other experiments); Vr_T = Vriesea splenriet, basal segments of tank leaves (plants of the same size as used in other experiments); Gz_S = Guzmania monostachia, plant size 2–4 cm; Gz_M = Guzmania monostachia, plant size 8–12 cm; Gz_L = Guzmania monostachia, plant size 22–25 cm; Wr_S = Werauhia sanguinolenta, plant size 2–4 cm; Wr_L = Werauhia sanguinolenta, plant size 16–18 cm; Tf_S = Tillandsia fasciculata, plant size 1–3 cm; Tf_L = Tillandsia fasciculata, plant size 14–18 cm; Ts_S = Tillandsia subulifera, plant size 1–3 cm; Ts_M = Tillandsia subulifera, plant size 8–12 cm; Tx_S = Tillandsia flexuosa, plant size 2–4 cm. The regression equation is: y=7·45x−10³ (1–e^{−2·8×10−4x}), r²=0·99.

Fig. 5.

Distribution of labelled rubidium in leaves, stems and roots of Vriesea splenriet. Experimental details for the uptake from tanks as described in Fig. 1, except that tanks were supplied with 0·5 mm unlabelled RbCl. After complete uptake of Rb⁺, tanks were watered only. After 1 and 9 d, plants were harvested and cut into small sections. Amounts of rubidium were calculated from the label in these sections. Leaves are numbered according to their age (A1 = oldest, non-senescent leaf). During ontogenetic development, the length of successive leaves is increasing in Vriesea. Thereby, fully grown adult leaves (A1–A12) can be distinguished from growing leaves (G13–G16) by comparing the length of leaves. Data are means ± s.d.; n = 4.

Fig. 6.

Distribution of potassium in leaves of Vriesea splenriet after 250 d of growth with and without potassium. Plants, which had been fertilized before the experiment, were grown under otherwise identical conditions in the greenhouse. Leaves are numbered according to their age. A1 was the oldest adult and A12 the youngest fully developed leaf. G13–G16 are still growing leaves. Data are means ± s.d.; n = 4.