MBE Advance Access published online on July 3, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm133
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Research Article |
Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 million years ago
* Research Center for Biodiversity, Academia Sinica, Taipei 115, Taiwan
Institute of Information Science, Academia Sinica, Taipei 115, Taiwan
¶ School of Forestry and Resource Conservation, National Taiwan University, Taipei 106, Taiwan
Corresponding author: Email: smchaw{at}sinica.edu.tw, Phone: 886-2-27892887; Fax: 886-2-27827954
Received for publication April 3, 2007. Revision received June 21, 2007. Accepted for publication June 25, 2007.
With the completion of the first gymnosperm mitochondrial genome (mtDNA) from Cycas taitungensis and the availability of more mtDNA taxa in the past five years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in eleven plants, including two algae, one liverwort, one moss, one gymnosperm, three monocots, and three eudicots. By using shared gene order and boundaries between different mtpts as the criterion, the timing of cpDNA transfer during plant evolution was estimated from the phylogenetic tree reconstructed independently from concatenated protein-coding genes of eleven available mtDNAs. Several interesting findings emerged. First, frequent DNA transfer from cpDNA to mtDNA occurred at least as far back as the common ancestor of extant gymnosperms and angiosperms, about 300 million years ago (MYA). The oldest mtpt is trnV(uac)-trnM(cau)-atpE-atpB-rbcL. Three other mtpts—psaA-psaB, rps19-trnH(gug)-rpl2-rpl23 and psbE-psbF—were dated to the common ancestor of extant angiosperms, at least 150 MYA. However, all protein-coding genes of mtpts have degenerated since their first transfer. Therefore, mtpts contribute nothing to the functioning of mtDNA but junk sequences. We discovered that the cpDNA transfers have occurred randomly at any positions of the cpDNAs except in the Cycas, the cp-derived protein-coding sequences of which were uniquely transferred from the LSC region. We provide strong evidence that the cp-derived tRNA-trnM(cau) is the only mtpt (1 out of 3 cp-derived tRNA shared by seed plants) truly transferred from cpDNA to mtDNA since the time of the common ancestor of extant gymnosperms and angiosperms. Our observations support Richly and Leister's (2004) proposition that "primary insertions of organellar DNAs are large and then diverge and fragment over evolutionary time."
Key Words: chloroplast genome • mitochondrial genome • mtpt • gene transfer • seed plants
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