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J. Biol. Chem., Vol. 280, Issue 22, 21531-21538, June 3, 2005

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Identical Hik-Rre Systems Are Involved in Perception and Transduction of Salt Signals and Hyperosmotic Signals but Regulate the Expression of Individual Genes to Different Extents in Synechocystis^*

Maria A. Shoumskaya¶, Kalyanee Paithoonrangsarid¶||, Yu Kanesaki, Dmitry A. Los, Vladislav V. Zinchenko**, Morakot Tanticharoen||, Iwane Suzuki, and Norio Murata

From the Division of Cellular Regulation, National Institute for Basic Biology, Okazaki 444-8585, Japan, Institute of Plant Physiology, Russian Academy of Sciences, Moscow 127276, Russia, ^||National Center for Genetic Engineering and Biotechnology, Bangkok 12120, Thailand, ^**Department of Genetics, Moscow State University, Moscow 119899, Russia, and Department of Molecular Biomechanics, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan

In previous studies, we characterized five histidine kinases (Hiks) and the cognate response regulators (Rres) that control the expression of 70% of the hyperosmotic stress-inducible genes in the cyanobacterium Synechocystis sp. PCC 6803. In the present study, we screened a gene knock-out library of Rres by RNA slot-blot hybridization and with a genome-wide DNA microarray and identified three Hik-Rre systems, namely, Hik33-Rre31, Hik10-Rre3, and Hik16-Hik41-Rre17, as well as another system that included Rre1, that were involved in perception of salt stress and transduction of the signal. We found that these Hik-Rre systems were identical to those that were involved in perception and transduction of the hyperosmotic stress signal. We compared the induction factors of the salt stress- and hyperosmotic stress-inducible genes that are located downstream of each system and found that these genes responded to the two kinds of stress to different respective extents. In addition, the Hik33-Rre31 system regulated the expression of genes that were specifically induced by hyperosmotic stress, whereas the system that included Rre1 regulated the expression of one or two genes that were specifically induced either by salt stress or by hyperosmotic stress. Our observations suggest that the perception of salt and hyperosmotic stress by the Hik-Rre systems is complex and that salt stress and hyperosmotic stress are perceived as distinct signals by the Hik-Rre systems.

Received for publication, October 27, 2004 , and in revised form, March 31, 2005.

^* This work was supported by Grants-in-aid for Scientific Research 14086207 (to N. M.) and 15013260 (to I. S.) from the Ministry of Education, Science, Culture, Japan and by Grant 13854002 (to N. M.) from the Japan Society for the Promotion of Science. It was also supported by the Program for Cooperative Research on the Stress Tolerance of Plants of the National Institute for Basic Biology, Japan and by grants from the Russian Foundation for Basic Research (03-04-48581) and from the program for "Molecular and Cellular Biology" of the Russian Academy of Sciences (to D. A. L.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ Both authors contributed equally to this work.

To whom correspondence should be addressed. Tel./Fax: 81-557-85-5205; E-mail: murata{at}nibb.ac.jp.

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