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Plant Physiol, November 2000, Vol. 124, pp. 991-1006

Aluminum-Induced 13--D-Glucan Inhibits Cell-to-Cell Trafficking of Molecules through Plasmodesmata. A New Mechanism of Aluminum Toxicity in Plants¹

Mayandi Sivaguru,² Toru Fujiwara, Josef amaj, Frantiek Baluka, Zhenming Yang, Hiroki Osawa, Takanori Maeda, Tomoko Mori, Dieter Volkmann, and Hideaki Matsumoto^*

Research Institute for Bioresources, Okayama University, Kurashiki 710-0046, Japan (M.S., Z.Y., H.O., T. Maeda, H.M.); Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan (T.F., T. Mori); Precursory Research for Embryonic Science and Technology, Japan Science and Technology Corporation, JST, Chiba 263-1123, Japan (T.F.); Department of Agronomy, Institute of Plant Genetics and Biotechnology, Slovak Academy of Sciences, 950 07 Nitra, Slovakia (J..); Department of Plant Cell Biology, Rheinische Friedrich-Wilhelms-Universität Bonn, D-53115 Bonn, Germany (F.B., D.V.); Bio-Oriented Technology Research Advancement Institution, Omiya 331-8537, Japan (H.O); and Changchun University of Agriculture and Animal Sciences, Changchun, 130062, Peoples Republic of China (Z.Y.)

Symplastic intercellular transport in plants is achieved by plasmodesmata (PD). These cytoplasmic channels are well known to interconnect plant cells to facilitate intercellular movement of water, nutrients, and signaling molecules including hormones. However, it is not known whether Al may affect this cell-to-cell transport process, which is a critical feature for roots as organs of nutrient/water uptake. We have microinjected the dye lucifer yellow carbohydrazide into peripheral root cells of an Al-sensitive wheat (Triticum aestivum cv Scout 66) either before or after Al treatment and followed the cell-to-cell dye-coupling through PD. Here we show that the Al-induced root growth inhibition is closely associated with the Al-induced blockage of cell-to-cell dye coupling. Immunofluorescence combined with immuno-electron microscopic techniques using monoclonal antibodies against 13--D-glucan (callose) revealed circumstantial evidence that Al-induced callose deposition at PD may responsible for this blockage of symplastic transport. Use of 2-deoxy-D-glucose, a callose synthesis inhibitor, allowed us to demonstrate that a reduction in callose particles correlated well with the improved dye-coupling and reduced root growth inhibition. While assessing the tissue specificity of this Al effect, comparable responses were obtained from the dye-coupling pattern in tobacco (Nicotiana tabacum) mesophyll cells. Analyses of the Al-induced expression of PD-associated proteins, such as calreticulin and unconventional myosin VIII, showed enhanced fluorescence and co-localizations with callose deposits. These results suggest that Al-signal mediated localized alterations to calcium homeostasis may drive callose formation and PD closure. Our data demonstrate that extracellular Al-induced callose deposition at PD could effectively block symplastic transport and communication in higher plants.

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¹ This work was supported by the Program for the Promotion of Basic Research Activities in Innovative Biosciences (PROBRAIN); by the Ministry of Agriculture, Forest and Fisheries, Japan; by a Grant-in-Aid for General Scientific Research (grade A) from the Ministry of Education, Science, Sports and Culture, Japan (to H.M.); by the Ohara Foundation for Agricultural Sciences; by postdoctoral fellowships awarded by the Japan Society for the Promotion of Science (to M.S. and Z.Y.); and by the Alexander von Humboldt Foundation, Germany (to J..).

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

^* Corresponding author; e-mail hmatsumo{at}rib.okayama-u.ac.jp; fax 81-86-434-1249/1210.

© 2000 American Society of Plant Physiologists

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