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MBE Advance Access originally published online on July 3, 2007
Molecular Biology and Evolution 2007 24(9):2040-2048; doi:10.1093/molbev/msm133
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© The Author 2007. 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

Research Articles

Transfer of Chloroplast Genomic DNA to Mitochondrial Genome Occurred At Least 300 MYA

Daryi Wang*, Yu-Wei Wu{dagger}, Arthur Chun-Chieh Shih{dagger}, Chung-Shien Wu*,{ddagger}, Ya-Nan Wang{ddagger} and Shu-Miaw Chaw*

* Research Center for Biodiversity
{dagger} Institute of Information Science, Academia Sinica, Taipei 115, Taiwan
{ddagger} School of Forestry and Resource Conservation, National Taiwan University, Taipei 106, Taiwan

E-mail: smchaw{at}sinica.edu.tw.

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 5 years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in 11 plants, including 2 algae, 1 liverwort, 1 moss, 1 gymnosperm, 3 monocots, and 3 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 11 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 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. 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 the proposition of Richly and Leister (2004) 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


Dan Graur, Associate Editor


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