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J. Biol. Chem., Vol. 280, Issue 44, 37098-37106, November 4, 2005

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Inactivation of Organellar Glutamyl- and Seryl-tRNA Synthetases Leads to Developmental Arrest of Chloroplasts and Mitochondria in Higher Plants^*

Yu-Kyung Kim1, Jae-Yong Lee1, Hye Sun Cho, Sang Sook Lee2, Hyun Jung Ha¶, Sunghoon Kim||, Doil Choi3, and Hyun-Sook Pai4

From the Laboratory of Plant Genomics, Korea Research Institute of Bioscience and Biotechnology, Taejon 305-333, Korea, the Division of Bioscience and Bioinformatics, Myongji University, Yongin, Kyonggi-do 449-728, Korea, the ^¶Department of Biochemistry, Chungbuk University, Cheongju, Chungcheongbuk-do, Korea, and the ^||National Creative Research Initiatives Center for ARS Network, Seoul National University, Seoul 151-742, Korea

Aminoacyl-tRNA synthetases (ARSs) are key enzymes involved in protein translation, and both cytosolic and organellar forms are present in the genomes of eukaryotes. In this study, we investigated cellular effects of depletion of organellar forms of ARS using virus-induced gene silencing (VIGS) in Nicotiana benthamiana. VIGS of NbERS and NbSRS, which encode organellar GluRS and SerRS, respectively, resulted in a severe leaf-yellowing phenotype. The NbERS and NbSRS genes were ubiquitously expressed in plant tissues, and induced in response to light. Green fluorescent protein (GFP) fusion proteins of the full-length glutamyl-tRNA synthetase (ERS) and seryl-tRNA synthetase (SRS) of Arabidopsis and GFP fusions to the N-terminal extension of these proteins were all dualtargeted to chloroplasts and mitochondria. At the cell level, depletion of NbERS and NbSRS resulted in dramatically reduced numbers of chloroplasts with reduced sizes and chlorophyll content. The numbers and/or physiology of mitochondria were also severely affected. The abnormal chloroplasts lacked most of the thylakoid membranes and appeared to be degenerating, whereas some of them showed doublet morphology, indicating defective chloroplast division. Pulse-field gel electrophoresis analyses demonstrated that chloroplast DNA in subgenomic sizes is the predominant form in the abnormal chloroplasts. Interestingly, despite severe abnormalities in chloroplasts and mitochondria, expression of many nuclear genes encoding chloroplastor mitochondria-targeted proteins, and chlorophyll biosynthesis genes remained unchanged in the ERS and SRS VIGS lines. This is the first report to analyze the effect of ARS disruption on organelle development in plants.

Received for publication, May 2, 2005 , and in revised form, August 1, 2005.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AAY18610 [GenBank] .

^* This work was supported by grants from the Plant Diversity Research Center of the 21st Century Frontier Research Program (to H.-S. P. and D. C.) and the Molecular and Cellular BioDiscovery Program (H.-S. P.), which are funded by the Ministry of Science and Technology of the Korean government. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1 and S2.

¹ Both authors contributed equally to this work.

² Present address: Dept. of Genetics, 445 Henry Mall, University of Wisconsin-Madison, Madison, WI 53706-1574.

³ To whom correspondence may be addressed: Tel.: 82-42-860-4340; Fax: 82-42-860-4309; E-mail: doil{at}kribb.re.kr.

⁴ To whom correspondence may be addressed: Tel.: 82-31-330-6191; Fax: 82-31-335-8249; E-mail: hspai{at}mju.ac.kr.

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