Aluminum Toxicity in Roots

Abstract

The inhibition of root growth by aluminum (Al) is well established , yet a unifying mechanism for Al toxicity remains unclear. The association between cell growth and endogenously generated ionic currents measured in many different systems, including plant roots, suggests that these currents may be directing growth. A vibrating voltage microelectrode system was used to measure the net ionic currents at the apex of wheat (Triticum aestivum L.) roots from Al-tolerant and Al-sensitive cultivars. We examined the relationship between these currents and Al-induced inhibition of root growth. In the Al-sensitive cultivar, Scout 66, 10 micromolar Al (pH 4.5) began to inhibit the net current and root elongation within 1 to 3 hours. These changes occurred concurrently in 75% of experiments. A significant correlation was found between current magnitude and the rate of root growth when data were pooled. No changes in either current magnitude or growth rate were observed in similar experiments using the Al-tolerant cultivar Atlas 66. Measurements with ion-selective microelectrodes suggested that H' influx was responsible for most of the current at the apex, with smaller contributions from Ca2" and Cl fluxes. In 50% of experiments , Al began to inhibit the net Ho influx in Scout 66 roots at the same time that growth was affected. However, in more than 25% of cases, Al-induced inhibition of growth rate occurred before any sustained decrease in the current or H' flux. Although showing a correlation between growth and current or H' fluxes, these data do not suggest a mechanistic association between these processes. We conclude that the inhibition of root growth by Al is not caused by the reduction in current or H' influx at the root apex. Al2 toxicity has been identified as one of the most important factors limiting plant growth in acid soils (5). Although a wide range of Al-related effects have been described in plants ' P.R.R. 2Apart from the Al3" cation, aluminum has the potential to form various hydroxy-aluminum and polynuclear species in solution. The available evidence suggests that the A13+ cation is phytotoxic, but it is unclear whether other hydroxy-aluminum species are also toxic (15). In this text, we denote aluminum as Al, without implying a specific aluminum species. 1193 (5, 30, 32), it is unclear whether any represent primary responses to Al toxicity. An early and dramatic symptom of Al phytotoxicity is inhibition of root growth, and with extended exposure (days), the roots thicken and become stubby and darker in color. The vibrating probe technique (12) has been used by many investigators to demonstrate a correlation between cell growth and endogenously generated transcellular ionic currents (8, 13, 27, 28). In several single-cell systems exhibiting tip growth (pollen tubes, root hairs, algal rhizoids, fungal hyphae), an inward current of between 0.1 and 5.0 uA cm-2 enters the tip region and a smaller, more diffuse current leaves the cell farther back. It is generally thought that separation of membrane-bound transport systems (separated either spatially or operationally) generate these transcellular currents (8, 28), a net influx of cations (or efflux of anions) being localized at the tip and a net efflux of cations (or influx of anions) occurring back from the tip. Clues to the identity of these ions can be obtained by manipulating the ionic composition of the bathing solution and monitoring changes in the measured current. However, this procedure is not always conclusive and may potentially give misleading results , especially in the case of Ca2" (7; see 'Discussion'). Because an association between transcellular currents and polarized growth has been described in a diverse range of plant systems, some workers have suggested that these currents , or perhaps the ions carrying the currents, are directing growth in some way (13, 27). Root elongation is not a true example of tip growth. Apart from being multicellular, they have two meristems: the root meristem proper and a second meristem directing new cells forward to maintain the root cap. However, roots do elongate in a polarized manner, and current pattems, similar to those described above for tip-growing systems, have been detected around roots of seedlings from at least five different families (20, 33). Net current enters the root apex (root cap, meristem, and part of the elongation zone) and leaves through the mature tissue. In roots of Zea mays, Miller and Gow (21) found that treatments that stimulated root growth (low pH, fusicoccin) were associated with an increase in the inward current at the root tip and elongation zones, whereas treatments that inhibited root growth (high pH, IAA) reduced the current magnitude. Furthermore , Miller et al. (23) showed that localized areas of