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J. Biol. Chem., Vol. 282, Issue 14, 10773-10782, April 6, 2007

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A Pentatricopeptide Repeat Protein Is Required for RNA Processing of clpP Pre-mRNA in Moss Chloroplasts^*

Mitsuru Hattori, Hiroshi Miyake, and Mamoru Sugita¹

From the Center for Gene Research, Nagoya University, Furo-cho 1, Chikusa-ku, Nagoya 464-8602 and the Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan

Pentatricopeptide repeat (PPR) proteins are encoded by the nuclear genome as a large gene family in land plants. PPR proteins play essential roles in organelle-related functions, mostly in RNA-processing steps in plastids and mitochondria. In the moss Physcomitrella patens, there is also a large gene family, but the moss PPR proteins are likely to be divergent from those of higher plants. To investigate the function of plastid PPR proteins, we have generated and characterized a PPR protein gene disruptant of P. patens. The PPR531-11-disrupted mosses displayed abnormal phenotypic characteristics, such as a significantly smaller protonemal colony, different chloroplast morphology, and incomplete thylakoid membrane formation. In addition, the quantum yield of photosystem II was reduced in the disrupted mosses. To further investigate whether disruption of the PPR531-11 gene affects chloroplast gene expression, we performed Northern blot and reverse transcription polymerase chain reaction analyses. These analyses revealed that PPR531-11 has a role in intergenic RNA cleavage between clpP and 5'-rps12 and in the splicing of clpP pre-mRNA. Western blot analysis showed that disruption of PPR531-11 resulted in a reduced level of ClpP, photosystem II reaction center protein D1, and the stromal enzyme, ribulose-bisphosphate carboxylase/oxygenase. These reductions might result in the severely retarded growth of the protonemal colony. Taken together, we propose a model where PPR531-11 function affects the steady-state level of ClpP, which regulates the formation and maintenance of thylakoid membranes in chloroplasts. This is the first evidence of a PPR protein controlling the protein expression level of ClpP.

Received for publication, August 22, 2006 , and in revised form, January 12, 2007.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AB267806 [GenBank] and AB267854 [GenBank] .

^* This work was supported by the Ministry of Education, Culture, Sports, Science, and Technology (Grant-in-Aid 14340252 to M. S.), by the Japan Society for the Promotion of Science Research Fellowships for Young Scientists (to M. H.), and by a research grant from Sekisui Chemical Co. Ltd. (to M. S.). 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.: 81-52-789-3080; Fax: 81-52-789-3080; E-mail: sugita{at}gene.nagoya-u.ac.jp.

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