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Plant Physiol, August 2001, Vol. 126, pp. 1381-1390

Aluminum Inhibits the H+-ATPase Activity by Permanently Altering the Plasma Membrane Surface Potentials in Squash Roots1

Sung Ju Ahn, Mayandi Sivaguru,2 Hiroki Osawa, Gap Chae Chung, and Hideaki Matsumoto*

Research Institute for Bioresources, Okayama University, Chuo 2-20-1, Kurashiki 710-0046, Japan (S.J.A., M.S., H.O., H.M.); Department of Horticulture, Biotechnology Research Institute, College of Agriculture, Chonnam National University, Kwangju 500-757, Korea (S.J.A, G.C.C.); and Bio-Oriented Technology Research Advancement Institution, Omiya 331-8637, Japan (H.O.)

Although aluminum (AL) toxicity has been widely studied in monocotyledonous crop plants, the mechanism of Al impact on economically important dicotyledonous plants is poorly understood. Here, we report the spatial pattern of Al-induced root growth inhibition, which is closely associated with inhibition of H+-ATPase activity coupled with decreased surface negativity of plasma membrane (PM) vesicles isolated from apical 5-mm root segments of squash (Cucurbita pepo L. cv Tetsukabuto) plants. High-sensitivity growth measurements indicated that the central elongation zone, located 2 to 4 mm from the tip, was preferentially inhibited where high Al accumulation was found. The highest positive shifts (depolarization) in zeta potential of the isolated PM vesicles from 0- to 5-mm regions of Al-treated roots were corresponded to pronounced inhibition of H+-ATPase activity. The depolarization of PM vesicles isolated from Al-treated roots in response to added Al in vitro was less than that of control roots, suggesting, particularly in the first 5-mm root apex, a tight Al binding to PM target sites or irreversible alteration of PM properties upon Al treatment to intact plants. In line with these data, immunolocalization of H+-ATPase revealed decreases in tissue-specific H+-ATPase in the epidermal and cortex cells (2-3 mm from tip) following Al treatments. Our report provides the first circumstantial evidence for a zone-specific depolarization of PM surface potential coupled with inhibition of H+-ATPase activity. These effects may indicate a direct Al interaction with H+-ATPase from the cytoplasmic side of the PM.


1 This work was supported by the Program for the Promotion of Basic Research Activities in Innovative Biosciences; by the Ministry of Agriculture, Forests and Fisheries, Japan (to H.M.); by the Ministry of Education, Science, Sports and Culture of Japan (Grant-in-Aid for General Scientific Research [A] to H.M.); by the Japan (to H.M.)-Korea (to G.C.C.) Joint Research Project supported by the Japan Society for the Promotion Science and Korea Science and Engineering Foundation (grant no. 986-0500-001-2); by the Basic Scientific Cooperation Program "Research for the Future" Program; and by the Japan Society for the Promotion Science, Ohara Foundation for Agricultural Sciences (postdoctoral fellowship to M.S.).

2 Present address: Division of Biological Sciences, 109 Tucker Hall, University of Missouri, Columbia, MO 65211-7400.

* Corresponding author; e-mail hmatsumo{at}rib.okayama-u.ac.jp; fax 81-86-434-1249.

© 2001 American Society of Plant Physiologists



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