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MBE Advance Access published online on September 13, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl112
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted September 7, 2006

Research Article

Evidence for Transit Peptide Acquisition Through Duplication and Subsequent Frameshift Mutation of a Preexisting Protein Gene in Rice

Minoru Ueda 1, Masaru Fujimoto 2, Shin-ichi Arimura 2, Nobuhiro Tsutsumi 2, and Koh-ichi Kadowaki 1 *

1 Genetic Diversity Department, National Institute of Agrobiological Sciences, Kannondai 2-1-2, Tsukuba, Ibaraki 305-8602, Japan
2 Laboratory of Plant Molecular Genetics, Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657 Japan

* To whom correspondence should be addressed.
Koh-ichi Kadowaki, E-mail: kadowaki{at}affrc.go.jp


  Abstract

Many proteins synthesized in the cytosol are delivered to their appropriate compartments in the cell by specific targeting signals. Here, we provide new insight into the generation of the chloroplast targeting signal (called the transit peptide) in rice. First, we identified the mitochondrial ribosomal protein L13 (mt rpl13) gene on chromosome 5. Downstream of the gene, we identified a DNA fragment of 266 bp: a segment within a duplication of mt rpl13. The duplicated region was transcribed and found to encode an open reading frame (ORF) of 160 amino acids (orf160). The orf160 gene comprises C-terminal 60 amino acids derived from the mt rpl13 gene and N-terminal 100 amino acids derived from another duplicated fragment of a pentatricopeptide repeat (ppr)564 gene that encodes 564 amino acids with ppr motifs on chromosome 1. Examination of the localization of the ORF160 protein tagged with green fluorescent protein (GFP) showed that it is targeted to the chloroplasts. As such, ORF160 clearly contains a transit peptide. Interestingly, this was translated from the alternative reading frame of the duplicated fragment of ppr564. To confirm this, the reading frame of the ppr564 gene was shifted according to that of the orf160 gene, and the frameshifted ppr564 sequence was fused to the gene for GFP. The expressed GFP-fused protein was also located in the chloroplasts. These results provide clear evidence for the generation of the transit peptide through duplication and subsequent frameshifting of a reading frame of a preexisting protein gene. We also demonstrate the importance of sequence redundancy and frameshift mutation in this evolutionary process.

Keywords: frameshift mutation; transit peptide; plastid; mitochondria; ribosomal protein; rice.

The nucleotide sequence data reported in this paper have been deposited in the DDBJ/EMBL/GenBank database under accession number AB244817 (ppr564)


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