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First published online June 17, 2005; 10.1104/pp.104.059097

Plant Physiology 138:1409-1421 (2005)
© 2005 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION

The Histidine Kinase Hik34 Is Involved in Thermotolerance by Regulating the Expression of Heat Shock Genes in Synechocystis1,[w]

Iwane Suzuki2,*, Yu Kanesaki, Hidenori Hayashi, John J. Hall, William J. Simon, Antoni R. Slabas and Norio Murata

Division of Cellular Regulation, National Institute for Basic Biology, Myodaiji, Okazaki 444–8585, Japan (I.S., Y.K., N.M.); Department of Biomechanics, Graduate University of Advanced Studies, Myodaiji, Okazaki 444–8585, Japan (I.S., N.M.); Satellite Venture Business Laboratory, Ehime University, Matsuyama 790–8577, Japan (Y.K., H.H.); and School of Biological and Biomedical Sciences, University of Durham, Durham DH1 3LE, United Kingdom (J.J.H., W.J.S., A.R.S.)

Histidine kinases (Hiks) in Synechocystis sp. PCC 6803 are involved in the transduction of signals associated with various kinds of environmental stress. To examine the potential role in thermotolerance of Hiks, we used genome microarray analysis to screen a Hik knockout library for mutations that affected the expression of genes for heat shock proteins. Mutation of the hik34 gene enhanced the levels of transcripts of a number of heat shock genes, including htpG and groESL1. Overexpression of the hik34 gene repressed the expression of these heat shock genes. In addition, the cells with a mutant gene for Hik34 ({Delta}Hik34 cells) survived incubation at 48°C for 3 h, while wild-type cells and cells with mutations in other Hiks were killed. However, mutation of the hik34 gene had only an insignificant effect on the global expression of genes upon incubation of the mutant cells at 44°C for 20 min. Quantitative two-dimensional gel electrophoresis revealed that levels of GroES and HspA were elevated in {Delta}Hik34 cells after incubation of cells at 42°C for 60 min. We overexpressed recombinant Hik34 protein in Escherichia coli and purified it. We found that the protein was autophosphorylated in vitro at physiological temperatures, but not at elevated temperatures, such as 44°C. These results suggest that Hik34 might negatively regulate the expression of certain heat shock genes that might be related to thermotolerance in Synechocystis.

1 This work was supported by Grants-in-Aid for Scientific Research for Priority Areas (C) Genome Biology (grant no. 16013249 to I.S.) and for Priority Areas (grant no. 14086207 to N.M.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and by a Grant-in-Aid for Scientific Research (S; grant no. 13854002 to I.S. and N.M.) from the Japan Society for the Promotion of Science. This work was also supported by the Salt Science Research Foundation and by the National Institute for Basic Biology Cooperative Research Program on Stress-Tolerant Plants. A.R.S., J.J.H., and W.J.S. are supported by the Biotechnology and Biological Sciences Research Council (BBSRC). J.J.H. wishes to thank Amersham Biosciences, United Kingdom, for supporting a BBSRC Ph.D. Cooperative Awards in Science and Engineering studentship.

2 Present address: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tennodai, Tsukuba 305–8572, Japan.

[w] The online version of this article contains Web-only data.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.059097.

* Corresponding author; e-mail iwanes6803{at}biol.tsukuba.ac.jp; fax 81–29–853–4666.

Received December 28, 2004; returned for revision March 10, 2005; accepted March 22, 2005.




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