Against the traffic: The first evidence for mitochondrial DNA transfer into the plastid genome

Authors: IORIZZO, MASSIMO - University Of Wisconsin; GRZEBELUS, DARIUSZ - Agricultural University Of Poland; Senalik, Douglas; SZKLARCZYK, MAREK - Agricultural University Of Poland; Spooner, David; Simon, Philipp

Submitted to: Mobile Genetic Elements
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/14/2012
Publication Date: 12/1/2012
Publication URL: https://handle.nal.usda.gov/10113/56711
Citation: Iorizzo, M., Grzebelus, D., Senalik, D.A., Szklarczyk, M., Spooner, D.M., Simon, P.W. 2012. Against the traffic: The first evidence for mitochondrial DNA transfer into the plastid genome. Mobile Genetic Elements. 2(6):261-266.

Interpretive Summary: DNA is the genetic material in all organisms that makes up genes. Most DNA is located in chromosomes, but in plants there is a small amount of DNA in two sub-cellular compartments: the mitochondria and the plastids. There is some research evidence over the last several decades that in rare cases DNA has moved between the chromosomes, mitochondria, and plastids. In earlier research we had discovered evidence that DNA in the carrot mitochondrion has moved to the carrot plastid, the first report of DNA transfer into plastid genomes of higher plants. In this current research we discuss the mechanisms that might be able to account for this DNA movement. We provide evidence that there are certain specific DNA sequences in the carrot plastid that are always associated with a process called ‘transposition’. The transposition process occurs widely in plants and animals, and results in DNA movement, but this is the first evidence for movement from mitochondria to plastid. This study is of interest to biologists, geneticists, plant scientists, and plant breeders.

Technical Abstract: Transfer of DNA between different compartments of the plant cell, i.e. plastid, mitochondrion and nucleus, is a well-known phenomenon in plant evolution. Six directions of inter-compartmental DNA migration are possible in theory, however only four of them have been previously reported. These include frequent cases of mitochondrion and plastid to nucleus transfer, and plastid to mitochondrion transfer, and rare nucleus to mitochondrion migrations. The connection between the plastid and mitochondrial genomes in flowering plants has been viewed as a one way road. Contrary to these observations we found that a sequence widespread in the carrot mitochondrial genome, designated as DcMP, was transferred to the plastid genome of a carrot ancestor. Interestingly, DcMP was integrated into a tRNA promoter of the plastid trnV gene, replacing the original promoter sequence. The rearrangement of the plastid genome is specific for carrot and closely related species belonging Scandiceae clade. The structure of the sequence and the presence of a 6 nt target site duplication led us to speculate that the transfer was a result of a transposition event of a non-LTR retrotransposon. These findings open interesting questions about the evolution of organellar genomes and mobile genetic elements and provide a useful plastid marker to phylogenetically delineate species relationships within the Scandiceae clade.