Plant Cell Advance Online Publication
Published on October 13, 2006; 10.1105/tpc.106.046110
Received July 26, 2006
Returned for revision August 23, 2006
Accepted September 18, 2006
A Pentatricopeptide Repeat Protein Facilitates the trans-Splicing of the Maize Chloroplast rps12 Pre-mRNA
Christian Schmitz-Linneweber 1, Rosalind E. Williams-Carrier 1, Pascale M. Williams-Voelker 1, Tiffany S. Kroeger 1, Athea Vichas 1, and Alice Barkan 1*
1 Institute of Molecular Biology, University of Oregon, Eugene, Oregon 97403
* To whom correspondence should be addressed. E-mail: abarkan{at}molbio.uoregon.edu.
The pentatricopeptide repeat (PPR) is a degenerate 35-amino acid repeat motif that is widely distributed among eukaryotes. Genetic, biochemical, and bioinformatic data suggest that many PPR proteins influence specific posttranscriptional steps in mitochondrial or chloroplast gene expression and that they may typically bind RNA. However, biological functions have been determined for only a few PPR proteins, and with few exceptions, substrate RNAs are unknown. To gain insight into the functions and substrates of the PPR protein family, we characterized the maize (Zea mays) nuclear gene ppr4, which encodes a chloroplast-targeted protein harboring both a PPR tract and an RNA recognition motif. Microarray analysis of RNA that coimmunoprecipitates with PPR4 showed that PPR4 is associated in vivo with the first intron of the plastid rps12 pre-mRNA, a group II intron that is transcribed in segments and spliced in trans. ppr4 mutants were recovered through a reverse-genetic screen and shown to be defective for rps12 trans-splicing. The observations that PPR4 is associated in vivo with rps12-intron 1 and that it is also required for its splicing demonstrate that PPR4 is an rps12 trans-splicing factor. These findings add trans-splicing to the list of RNA-related functions associated with PPR proteins and suggest that plastid group II trans-splicing is performed by different machineries in vascular plants and algae.
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|
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|
|
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|
|
|
|
|
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|
|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
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