Uptake of aluminium by plant cells

Abstract

SUMMARY The question of intracellular or extracellular primary lesion in the Al toxicity syndrome is unresolved. One of the crucial points for answering that question is quantification of Al fluxes across the plasma membrane within seconds or minutes of exposure of roots to Al, i.e. concurrent with or preceding the first symptoms of Al toxicity. A review of the available literature on Al uptake shows that there is abundant information on Al accumulation in root tissues only after the relatively prolonged uptake period, ranging from 30 min to over 24 h. Most of these reports either assume or claim explicitly that intracellular Al was measured, even though Al ions are bound strongly to negative charges in the apoplasm. Therefore, an effective and complete desorption of apoplasmic Al after the uptake period is crucial for measurements of intracellular Al. However, published studies do not seem to have desorbed cell‐wall‐bound Al appropriately. Recent studies with giant algal cells of Chara corallina, where physical separation of cell wall and cytoplasm after the uptake period can be achieved surgically, showed that desorption of Al from the apoplasm, even employing a wider variety of desorbents and more stringent conditions than in any of the previously published reports, cannot be achieved completely within 5 h. Consequently, measured rates of uptake of Al across the plasma membrane of intact Chara cells employing the cell wall/cytoplasm separation technique are up to several orders of magnitude lower than previously published values in which cell‐wall Al was attributed to the transmembrane uptake component. Although there is no doubt that Al does cross the plasma membrane, no information exists about which Al species or complexes take part in the transmembrane flux, mainly because of complexities inherent in Al speciation at the solution/ion exchanger (i.e. the cell wall and the membrane) interface. Similarly, it is not known which membrane transporters are involved in transport of Al across the plasma membrane. The Al‐resistant plant genotypes generally accumulate less Al in the root tips than do the Al‐sensitive genotypes. No direct relationship, however, appears to exist between increased organic acid extrusion as a mechanism of resistance to Al and decreased transmembrane flux of Al. Al‐accumulator plant species accumulate relatively large amounts of Al in their tissues without having a greater Al uptake rate than non‐accumulator genotypes. Progress in deciphering structural and functional aspects of transport of Al across the plasma membrane of intact plant cells will rely on using giant algal cells in which physical separation of the cell wall and the cytoplasm can be achieved, because, at present, there is no reliable quantitative method which can overcome problems presented by a relatively large apoplasmic Al pool remaining after desorption of intact root cells of higher plants.

Aluminium effects on microtubule organization in dividing root‐tip cells of Triticum turgidum. I. Mitotic cells

“…Externally applied Al rapidly binds to certain sites of the root-tip apoplast (Horst, 1995 ;Rengel, 1996). However, shortly afterwards small quantities of Al, which in the case of soyabean root-tip cells vary between 30 and 70 mmol g −" f.wt, enter the cytoplasm (Lazof et al, 1994), interfering with many signal-transduction pathways (Kochian, 1995 ;Kochian & Jones, 1997).…”

“…(1) Disturbance of cytosolic Ca# + homoeostasis : Al modifies the concentration of free cytosolic Ca# + (Rengel, 1996 ;Kochian & Jones, 1997 ;Jones et al, 1998a,b), affecting the function of the plasmalemma pumps transporting Ca# + (Pineros & Tester, 1995 ;Jones et al, 1998a). Aluminium may also block Ca# + channels residing in other biomembranes (Kochian & Jones, 1997).…”

“…(2) Inhibition of calmodulin activity : Al$ + binds stoichiometrically to Ca# + -binding sites in calmodulin with a 10-fold higher affinity than Ca# + , and elicits dramatic conformational changes in calmodulin that should inhibit its ability to activate other enzymes (Siegel & Haug, 1983 ;Rengel, 1992Rengel, , 1996Kochian, 1995 ;Kochian & Jones, 1997).…”

Nitrogen and phosphorus acquisition by the mycelium of the ectomycorrhizal fungus Paxillus involutus and its effect on host nutrition

“…Thus, the resulting mass flow of water through the sand can be assumed to be similar in both treatments. Aluminium applied to the hyphal compartment was used as a label for the estimation of mass flow, as it is readily adsorbed by plant cell walls (Horst, 1995 ;Rengel, 1996), and even small amounts in the nutrient solution accumulate in the plant material.…”

Aluminum Accumulation at Nuclei of Cells in the Root Tip. Fluorescence Detection Using Lumogallion and Confocal Laser Scanning Microscopy

“…Effects likely are located at the root tip itself (Ryan et al, 1993;Sivaguru and Horst, 1998), and several types of regulatory factors are likely to be involved (Kochian, 1995). Convincing arguments have been advanced for toxicity mechanisms operating in the root apoplast (Horst, 1995;Rengel, 1996) and symplasm (Jones and Kochian, 1995;Kochian, 1995;Jones et al, 1998), at the plasma membrane (Barceló et al, 1996), as well as involving complex interactions at the cell wall/plasma membrane/cytoskeleton continuum (Sivaguru et al, 1999).…”