Multiple Aluminum-Resistance Mechanisms in Wheat (Roles of Root Apical Phosphate and Malate Exudation)

Abstract

Although it is well known that aluminum (AI) resistance in wheat (Trificum aestivum) is multigenic, physiological evidence for multiple mechanisms of AI resistance has not yet been documented. l h e role of root apical phosphate and malate exudation in AI resistance was investigated i n two wheat cultivars (AI-resistant Atlas and AI-sensitive Scout) and two near-isogenic lines (AI-resistant E13 and AI-sensitive ES3). I n Atlas AI resistance is multigenic, whereas in E13 resistance is conditioned by the single Alfl locus. Based on rootgrowth experiments, Atlas was found to be 3-fold more resistant in 20 PM AI than ET3. Root-exudation experiments were conducted under sterile conditions; a large malate efflux localized to the root apex was observed only in Atlas and in ET3 and only i n the presence of AI (5 and 20 p~) .Furthermore, the more AI-resistant Atlas exhibited a constitutive phosphate release localized to the root apex. As predicted from the formation constants for the AI-malate and AI-phosphate complexes, the addition of either ligand to the root bathing solution alleviated AI inhibition of root growth in AI-sensitive Scout. These results provide physiological evidence that AI resistance in Atlas is conditioned by at least two genes. I n addition to the alf locus that controls AI-induced malate release from the root apex, other genetic loci appear to control constitutive phosphate release from the apex. We suggest that both exudation processes act in concert to enhance AI exclusion and AI resistance i n Atlas.A1 toxicity is one of the major factors that limits the productivity of crop plants in acid soils. A number of crop species and cultivars exhibit significant genetically based variability in their response to the toxic levels of soil A1 (Kochian, 1995). This variability has served as the basis for a considerable amount of recent research on the underlying mechanisms that result in crop A1 resistance. We are beginning to understand the cellular processes that confer A1 resistance in plants. Most of the recent work has focused on A1 exclusion from the root apex as a primary mechanism of A1 resistance (Kochian, 1995).Root exudation of organic acids that can chelate A13+ in the rhzosphere and, thus, detoxify A1 was first reported in an

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

“…The involvement of rhizosphere alkalinization (Degenhardt et al, 1998), efflux of Al from the symplasm (Ezaki et al, 1999), and decreased cell-surface negativity (Wagatsuma and Akiba, 1989) are also possible. There is evidence indicating that Al tolerance in PI 416937 involves three to five genes (Bianchi-Hall et al, 1998), which is consistent with concomitant operation of multiple Al-tolerance mechanisms, as evidently occurs in wheat (Pellet et al, 1996).…”

“…Root tip Al concentrations were found to be lower in Al-tolerant genotypes with other plant species as well (Rincó n and Gonzalez, 1992;Tice et al, 1992;Delhaize et al, 1993a;Ryan et al, 1997;Samuels et al, 1997;Larsen et al, 1998). A myriad of processes could contribute to Al exclusion from the meristematic cell region, including increased secretion of mucilage (Horst et al, 1982;Crawford and Wilkens, 1997), polypeptides (Basu et al, 1999), inorganic phosphate (Pellet et al, 1996), and organic acids (Delhaize et al, 1993b;Basu et al, 1994;Delhaize and Ryan, 1995;Pellet et al, 1995;Larsen et al, 1998). The involvement of rhizosphere alkalinization (Degenhardt et al, 1998), efflux of Al from the symplasm (Ezaki et al, 1999), and decreased cell-surface negativity (Wagatsuma and Akiba, 1989) are also possible.…”

Sorption of Aluminum to Plasma Membrane Vesicles Isolated from Roots of Scout 66 and Atlas 66 Cultivars of Wheat

“…According to our estimates, the differences in PM surface negativity and AI sorptive capacity, whatever the cause of the latter, probably account for some of the difference in genotypic sensitivity to AI3+, but the greater part of that difference may arise because malate and phosphate secretion by cv Atlas root tips reduces the amount of AI3+ that can reach the PM (Huang et al, 1996;Pellet et al, 1996). The evidence that malate release is a general mechanism for tolerance in wheat is reasonably strong now.…”

Aluminum-Resistant Arabidopsis Mutants That Exhibit Altered Patterns of Aluminum Accumulation and Organic Acid Release from Roots1

“…Because plant anion channels can be regulated by a number of external and internal factors (Ebel and Cosio, 1994;Schroeder, 1995;Thomine et al, 1995;Ward et al, 1995), it is possible that at least in wheat and maize, Al may play a role in anion-channel gating (Delhaize et al, 1993b;Pellet et al, 1995Pellet et al, , 1996Ryan et al, 1995aRyan et al, , 1995b. Support for this possibility comes from the results of a recent study by Ryan et al (1997), which were based on an electrophysiological (patch-clamp) analysis of protoplasts isolated from the root apex of the Al-resistant wheat line used to initially demonstrate Al-inducible malate release.…”

“…More recently, it was shown that constitutive phosphate release might operate in conjunction with Al-induced organic release to confer a greater degree of Al resistance in certain wheat genotypes (Pellet et al, 1996). Another mechanism of Al exclusion that is frequently proposed is a root-mediated elevation in the pH of the rhizosphere adjacent to the root apex (Kochian, 1995).…”