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First published online July 17, 2003; 10.1104/pp.103.022129

Plant Physiology 132:2256-2266 (2003)
© 2003 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION

Aluminum-Induced Gene Expression and Protein Localization of a Cell Wall-Associated Receptor Kinase in Arabidopsis1

Mayandi Sivaguru, Bunichi Ezaki, Zheng-Hui He, Hongyun Tong, Hiroki Osawa, Frantisek Baluska, Dieter Volkmann and Hideaki Matsumoto*

Molecular Cytology Core Facility, Molecular Biology Program, 2 Tucker Hall, University of Missouri, Columbia, Missouri 65211–7400 (M.S.); Research Institute for Bioresources, Okayama University, Chuo 2–20–1, Kurashiki 710–0046, Japan (B.E., H.O., H.M.); Department of Biology, San Francisco State University, San Francisco, California 94132 (Z.-H.H., H.T.); and Department of Plant Cell Biology, Rheinische Friedrich-Wilhelms University of Bonn, Kirchalle 1, D–53115 Bonn, Germany (F.B., D.V.)

Here, we report the aluminum (Al)-induced organ-specific expression of a WAK1 (cell wall-associated receptor kinase 1) gene and cell type-specific localization of WAK proteins in Arabidopsis. WAK1-specific reverse transcriptase-polymerase chain reaction analysis revealed an Al-induced WAK1 gene expression in roots. Short- and long-term analysis of gene expression in root fractions showed a typical "on" and "off" pattern with a first peak at 3 h of Al exposure followed by a sharp decline at 6 h and a complete disappearance after 9 h of Al exposure, suggesting the WAK1 is a further representative of Al-induced early genes. In shoots, upon root Al exposure, an increased but stable WAK1 expression was observed. Using confocal microscopy, we visualized Al-induced closure of leaf stomata, consistent with previous suggestions that the Al stress primarily experienced in roots associated with the transfer of root-shoot signals. Elevated levels of WAK protein in root cells were observed through western blots after 6 h of Al exposure, indicating a lag time between the Al-induced WAK transcription and translation. WAK proteins are localized abundantly to peripheries of cortex cells within the elongation zone of the root apex. In these root cells, disintegration of cortical microtubules was observed after Al treatment but not after the Al analog lanthanum treatments. Tip-growing control root hairs, stem stomata, and leaf stomatal pores are characterized with high amounts of WAKs, suggesting WAKs are accumulating at plasma membrane domains, which suffer from mechanical stress and lack dense arrays of supporting cortical microtubules. Further, transgenic plants overexpressing WAK1 showed an enhanced Al tolerance in terms of root growth when compared with the wild-type plants, making the WAK1 one of the important candidates for plant defense against Al toxicity.

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 Japan Society for the Promotion of Science (postdoctoral fellowship to M.S.); and by the National Science Foundation (grant no. MCB–9985135 to Z.-H.H.).

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

Received February 16, 2003; returned for revision March 30, 2003; accepted May 12, 2003.




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