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Uptake, Transport and Accumulation of Nicotine by the Golden Potho (Epipremnum Aureum): the Central Role of Root Pressure

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Uptake, Transport and Accumulation of Nicotine by the Golden Potho (Epipremnum Aureum): the Central Role of Root Pressure ARTICLE IN PRESS Journal of Plant Physiology 162 (2005) 139—150 www.elsevier.de/jplph Uptake, transport and accumulation of nicotine by the Golden Potho (Epipremnum aureum): the central role of root pressure Manfred WeidnerÃ, Ralf Martins, Andrea Mu¨ller, Judith Simon, Heribert Schmitz Botanisches Institut, Universita¨t zu Ko¨ln, Gyrhofstrasse 15, Ko¨ln 50923, Germany Received 3 February 2004; accepted 19 July 2004 KEYWORDS Summary Epipremnum The roots of Epipremnum aureum, though not synthesizing nicotine themselves, take aureum; up exogenously fed nicotine as a xenobiotic. The alkaloid is subsequently translocated Golden potho; to the leaves, via the xylem path, where it accumulates in the mesophyll up to levels Nicotine uptake; comparable with nicotine-rich Nicotiana species. The Epipremnum plants accept Xenobiotics; nicotine only up to a distinct level; saturation is reached after about 10 days. All Ion trap; mature, non-senescent leaves accumulate the same amount of nicotine. By different Root pressure; experimental approaches, unequivocal evidence could be provided that root pressure Leaf senescence is the ‘translocative force’ for nicotine transport in E. aureum. Xylem sap exudates, collected from shoot stumps that were connected to an intact root system immersed in nicotine solution were analyzed for nicotine content. Nicotine uptake from the medium by the root and its subsequent transfer into the xylem of the shoot persisted for more than 10 h without measurable decline of the transport rate, provided the nicotine concentrations applied were p0.05%. In intact plants, where both components of water transport in the xylem — root pressure and transpirative water flow — are in operation, no surplus transport of nicotine from the roots into the leaves took place beyond the level observed in amputated plants. Under the influence of inhibitors of root respiration, nicotine uptake was halted slowly in case of oxygen deprivation and in case of cyanide, or it stopped very rapidly when CCCP,an uncoupler of mitochondrial ATP formation, was applied to the roots. This threshold of toxicity against the xenobiotic was established by dose effect curves for nicotine sensitivity of the roots for root respiration and by transpiration measurements. Leaves, bearing a heavy ‘nicotine load’, showed symptoms of senescence only after 3–6 weeks, as indicated by a decline in the chlorophyll content, the chl a/b ratio, and the maximal quantum yield efficiency (Fv/Fm), and by an increase in catalase activity. Our results ÃCorresponding author. Tel.: +49 221 470 3903; fax: +49 221 470 5062. E-mail address: [email protected] (M. Weidner). 0176-1617/$ - see front matter & 2004 Elsevier GmbH. All rights reserved. doi:10.1016/j.jplph.2004.07.012 ARTICLE IN PRESS 140 M. Weidner et al. provide insight into the mechanisms of uptake, transport and storage of nicotine as a xenobiotic. & 2004 Elsevier GmbH. All rights reserved. Introduction plants. Experiments were mostly carried out with well-rooted plants that had developed 4–6 new Originally, we observed that 14C nicotine fed to the leaves after vegetative propagation (cloning). roots of Epipremnum aureum was taken up easily by this ornamental plant, known as ‘Golden Potho’. General growth and incubation conditions Although E. aureum does not synthesize nicotine itself, considerable amounts of nicotine were For the experiments, the plants were transferred deposited in the leaves (Schmitz, 1995). Therefore, into 100 ml-Erlenmeyer-flasks or 250-ml beakers nicotine has to be considered a xenobiotic sub- containing 25–100 ml incubation medium, depend- stance (Sandermann, 1992; Martinoia et al., 2000) ing on the experiment; the roots were kept with respect to E. aureum. In contrast, Ficus submersed. The opening of the flasks/beakers was benjamina — the ‘weeping fig’ — , another favorite covered with aluminum foil or Parafilms wrapped plant for indoor greening purposes, does not at all around the stem in order to prevent evaporation. take up niocotine from a root medium (Schmitz, The incubation medium consisted of Knop’s nutri- 1995). Hence, we became interested in this ent solution (Hewitt, 1966); 0.03% chloroampheni- seemingly uncommon capability of E. aureum, col was included to suppress the growth of nicotine- which — to our knowledge — has not been reported consuming bacteria (Eberhardt, 1995). Alterna- before. Consequently, the present investigation tively, Hoagland No. 3 nutrient solution, supple- was initiated. Our main focus is directed on mented with Arnon’s A-4 micronutrient solution nicotine uptake and transport mechanisms and on (Hoagland and Arnon, 1950), was used. The nicotine storage in the leaves of E. aureum.A osmolality of the incubation media was major experimental tool was xylem sap analysis. 0.0570.02 osmol kgÀ1. Since this species exhibits pronounced and long- The dissociation equilibrium between the elec- lasting root pressure activity, it was possible to troneutral (nic) and the cationic form of nicotine collect xylem sap exudate for many hours. In this (nic+) depends on the pH of the solution (The Merck context, the effects of inhibition of root pressure Index, 1976). At pH 7, about 50% of the nicotine is via inhibitor-induced ATP deprivation of the root in the nic-form (electroneutral), calculated on the were also studied. Furthermore, we were inter- basis of an apparent pKa-value of 8.02 for nicotine, ested in the (stress) physiological consequences of whereas at pH 5.3 (the pH-value of E. aureum root nicotine accumulation in the leaves with respect to homogenates) only about 1% is in the apolar/ induced leaf senescence. lipophilic form according to the equation: ½nicþ pH À 8:02 ¼ log : (1) ½nic Materials and methods The pH-value of the incubation medium either Plant material adjusted to pH 7, which is the normal pH-value for nutrient solutions, or pH 5.3, which is the pH-value All experiments were carried out with the Golden of E. aureum root homogenates. Potho (devils ivy) E. aureum Lind and Andre (=Epipremnum pinnatum L.). Hydroponic plants of Pulse-chase incubation of intact plants with E. aureum were obtained from Geselka GmbH, 14C nicotine Ko¨ln, FRG. The mother plants were cloned, that is, they were fractioned into one-leaf stem cuttings Two days before the pulse-chase experiment was that were grown on Vermiculites for 10–12 weeks started, the E. aureum plants were removed from in the greenhouse at 725 1C under natural light the greenhouse and preadapted to the conditions of and, supplementary, with artificial white light the growth chamber, where the nicotine incubation (Phillips SON-T-AGRO 400; photon flux density (pulse) and the subsequent chase period were to be (PFD) approximately 500 mmol mÀ2 sÀ1). Commer- administered. The settings were as follows: 25 1C, cial fertilizer (‘Wuxal Super’; N/P/K 8:8:6 plus 70% relative humidity, continuous light (fluorescent micronutrients) was administered weekly to the tubes ‘cool white’), PFD was approximately ARTICLE IN PRESS Nicotine transport in Epipremnum aureum 141 150 mmol mÀ2 sÀ1. A 48 h nicotine pulse was admi- contained 0.05% (v/v) unlabeled nicotine. In order nistered to the roots by adding (pyrrolidone-2-14C)- to maintain a non-obstructed xylem sap exudation DL-nicotine to Knop’s medium (pH 7) to yield a final for an extended period of time, a 2 mm slice was concentration of 0.05% (v/v) on nicotine; the cut off the stump surface after every second xylem- specific activity was 2.4 MBq mmolÀ1 sap ‘harvest’. (7.4 kBq mlÀ1). During incubation, the flasks were agitated slowly on a shaker. At the end of the pulse Nicotine incubation of intact plants in the period the plants were either analyzed directly for s presence of inhibitors nicotine or were replanted into Vermiculite and watered with nicotine-free Knop’s medium for the E. aureum plants were transferred from the chase periods, applied. The harvested plant mate- Vermiculite into beakers that contained Hoagland’s rial was wrapped in punctured aluminum foil, deep- nutrient medium adjusted to pH 7. At this pH- frozen with liquid nitrogen (LN ), and stored at 2 value, the concentration of nic equals the concen- À20 1C until the analyses were carried out. Xylem tration of nic+ (see above). After preadaptation to sap aliquots were shock-frozen (LN /À20 1C) in 2 growth chamber conditions, 0.05% unlabeled nico- 1,5 ml tubes. tine was added. In addition, either KCN or CCCP The in vivo measuring of incorporated label of (carbonyl cyanide-m-chlorophenylhydrazone) was whole leaves was done with a large-window 14C included to yield a final concentration of 10À4 M xenon monitor (Contamat FHT 111 M; FAG Schwein- (cyanide) or 10À5 M (CCCP), respectively. In the furt, FRG). The counter was positioned 2 mm above third inhibition treatment, nitrogen instead of air the leaf surface. For one recording, three con- was bubbled through the incubation medium in secutive 2 min-measurements (Bq cmÀ2) of a cer- order to establish anoxic conditions. In case of the tain leaf were taken and averaged. The standard N treatment, a pinhole in the Parafilms cover errors were in the range of 2%. Due to the relatively 2 enabled the ventilated gas to escape. The tran- low 14C counting sensitivity inherent to this detec- spired water volume was determined by differen- tion method, the values do not represent the tial weighing of the whole setup (plants and absolute of incorporated labeled nicotine. How- beakers). Six plants plus six inhibitor-free controls ever, this fact does not distort the time curve of were used for each inhibition variant. labeling and the final distribution of incorporated After 24 h of incubation, all shoots were cut off 14C. An autoradiogram from a whole plant was about 5 cm above the root base and dissected. The obtained after a 2 day pulse, followed by a 10 day root bodies including the shoot stumps remained in chase period.
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