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Background  Many mitochondrial genes, especially ribosomal protein genes, have been frequently transferred as functional entities to the nucleus during plant evolution, often by an RNA-mediated process. A notable case of transfer involves the  rps14  gene of three grasses (rice, maize, and wheat), which has been relocated to the intron of the nuclear  sdh2  gene and which is expressed and targeted to the mitochondrion via alternative splicing and usage of the  sdh2  targeting peptide. Although this transfer occurred at least 50 million years ago, i.e., in a common ancestor of these three grasses, it is striking that expressed, nearly intact pseudogenes of  rps14  are retained in the mitochondrial genomes of both rice and wheat. To determine how ancient this transfer is, the extent to which mitochondrial  rps14  has been retained and is expressed in grasses, and whether other transfers of  rps14  have occurred in grasses and their relatives, we investigated the structure, expression, and phylogeny of mitochondrial and nuclear  rps14  genes from 32 additional genera of grasses and from 9 other members of the Poales.    Results  Filter hybridization experiments showed that  rps14  sequences are present in the mitochondrial genomes of all examined Poales except for members of the grass subfamily Panicoideae (to which maize belongs). However, PCR amplification and sequencing revealed that the mitochondrial  rps14  genes of all examined grasses (Poaceae), Cyperaceae, and Joinvilleaceae are pseudogenes, with all those from the Poaceae sharing two 4-NT frameshift deletions and all those from the Cyperaceae sharing a 5-NT insertion (only one member of the Joinvilleaceae was examined). cDNA analysis showed that all mitochondrial pseudogenes examined (from all three families) are transcribed, that most are RNA edited, and that surprisingly many of the edits are reverse (U→C) edits. Putatively nuclear copies of  rps14  were isolated from one to several members of each of these three Poales families. Multiple lines of evidence indicate that the nuclear genes are probably the products of three independent transfers.    Conclusion  The  rps14  gene has, most likely, been functionally transferred from the mitochondrion to the nucleus at least three times during the evolution of the Poales. The transfers in Cyperaceae and Poaceae are relatively ancient, occurring in the common ancestor of each family, roughly 80 million years ago, whereas the putative Joinvilleaceae transfer may be the most recent case of functional organelle-to-nucleus transfer yet described in any organism. Remarkably, nearly intact and expressed pseudogenes of  rps14  have persisted in the mitochondrial genomes of most lineages of Poaceae and Cyperaceae despite the antiquity of the transfers and of the frameshift and RNA editing mutations that mark the mitochondrial genes as pseudogenes. Such long-term, nearly pervasive survival of expressed, apparent pseudogenes is to our knowledge unparalleled in any genome. Such survival probably reflects a combination of factors, including the short length of  rps14 , its location immediately downstream of  rpl5  in most plants, and low rates of nucleotide substitutions and indels in plant mitochondrial DNAs. Their survival also raises the possibility that these  rps14  sequences may not actually be pseudogenes despite their appearance as such. Overall, these findings indicate that intracellular gene transfer may occur even more frequently in angiosperms than already recognized and that pseudogenes in plant mitochondrial genomes can be surprisingly resistant to forces that lead to gene loss and inactivation.

bmc evolutionary biology

Pervasive survival of expressed mitochondrial rps14 pseudogenes in grasses and their relatives for 80 million years following three functional transfers to the nucleus.