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J. Biol. Chem., Vol. 282, Issue 49, 35536-35545, December 7, 2007

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Calcium-activated (p)ppGpp Synthetase in Chloroplasts of Land Plants^*

Yuzuru Tozawa¹, Akira Nozawa, Takuya Kanno, Takakuni Narisawa, Shinji Masuda^¶, Koji Kasai^||, and Hideaki Nanamiya

From the Cell-Free Science and Technology Research Center and the Department of Applied Chemistry, Graduate School of Science and Engineering, Ehime University, 3 Bunkyo-cho, Matsuyama 890-8577, Japan, the ^¶Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta, Yokohama 226-8501, Japan, and the ^||Biotechnology Research Center, University of Tokyo, 1-1-1 Yayoi, Tokyo 113-8657, Japan

The genetic system of chloroplasts, including the machinery for transcription, translation, and DNA replication, exhibits substantial similarity to that of eubacteria. Chloroplasts are also thought to possess a system for generating guanosine 5'-triphosphate ((p)ppGpp), which triggers the stringent response in eubacteria, with genes encoding chloroplastic (p)ppGpp synthetase having been identified. We now describe the identification and characterization of genes (OsCRSH1, OsCRSH2, and OsCRSH3) for a novel type of (p)ppGpp synthetase in rice. The proteins encoded by these genes contain a putative chloroplast transit peptide at the NH₂ terminus, a central RelA-SpoT-like domain, and two EF-hand motifs at the COOH terminus. The recombinant OsCRSH1 protein was imported into chloroplasts in vitro, and genetic complementation analysis revealed that expression of OsCRSH1 suppressed the phenotype of an Escherichia coli mutant deficient in the RelA and SpoT enzymes. Biochemical analysis showed that the OsCRSH proteins possess (p)ppGpp synthetase activity that is dependent both on Ca²⁺ and on the EF-hand motifs. A data base search identified a CRSH homolog in the dicotyledon Arabidopsis thaliana, indicating that such genes are conserved among both monocotyledonous and dicotyledonous land plants. CRSH proteins thus likely function as Ca²⁺-activated (p)ppGpp synthetases in plant chloroplasts, implicating both Ca²⁺ and (p)ppGpp signaling in regulation of the genetic system of these organelles.

Received for publication, May 9, 2007 , and in revised form, October 11, 2007.

^* This work was supported by Rice Genome Project Grants MP-2115 and PR-1105 from the Ministry of Agriculture, Forestry, and Fisheries of Japan (to Y. T.) and Grant-in-aid for Scientific Research 19570042 (to Y. T.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. 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.

¹ To whom correspondence should be addressed. Tel.: 81-89-927-8274; Fax: 81-89-927-8276; E-mail: tozaway{at}ccr.ehime-u.ac.jp.

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