Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants

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Abstract

A central component of the endosymbiotic theory for the bacterial origin of the mitochondrion is that many of its genes were transferred to the nucleus. Most of this transfer occurred early in mitochondrial evolution1; functional transfer of mitochondrial genes has ceased in animals2. Although mitochondrial gene transfer continues to occur in plants3, no comprehensive study of the frequency and timing of transfers during plant evolution has been conducted. Here we report frequent loss (26 times) and transfer to the nucleus of the mitochondrial gene rps10 among 277 diverse angiosperms. Characterization of nuclear rps10 genes from 16 out of 26 loss lineages implies that many independent, RNA-mediated rps10 transfers occurred during recent angiosperm evolution; each of the genes may represent a separate functional gene transfer. Thus, rps10 has been transferred to the nucleus at a surprisingly high rate during angiosperm evolution. The structures of several nuclear rps10 genes reveal diverse mechanisms by which transferred genes become activated, including parasitism of pre-existing nuclear genes for mitochondrial or cytoplasmic proteins, and activation without gain of a mitochondrial targeting sequence.

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Figure 1: Southern blot hybridizations of 51 angiosperms (out of 277 examined in total) with the indicated angiosperm probes.
Figure 2: Sporadic loss of the mitochondrial rps10 gene among the surveyed angiosperms.
Figure 3: Partial sequence comparisons of three chimaeric nuclear rps10 genes and structures of seven nuclear rps10 genes.
Figure 4: Import of RPS10 proteins into isolated mitochondria.
Figure 5: Maximum likelihood trees of mitochondrial and nuclear rps10 nucleotide sequences.

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Acknowledgements

We thank W. Fischer, J. Logsdon, C. Parkinson, M. Rosenblueth, N. Schisler and K. Wolfe for reading the manuscript, and D. Swofford for allowing us to use a pre-release version of PAUP*. This study was supported by a United States Department of Agriculture graduate fellowship to K.L.A., grants to Y.L.Q. and J.D.P. from the NIH, and grants from the Australian Research Council to J.W.

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Correspondence to Jeffrey D. Palmer.

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