Intracellular gene transfer in action: Dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes

The respiratory gene cox2, normally present in the mitochondrion, was previ ously shown to have been functionally transferred to the nucleus during flo wering plant evolution, possibly during the diversification of legumes. To search for novel intermediate stages in the process of intracellular gene t ransfer and to assess the evolutionary timing and frequency of cox2 transfe r, activation, and inactivation, we examined nuclear and mitochondrial (mt) cox2 presence and expression in over 25 legume genera and mt cox2 presence in 392 genera. Transfer and activation of cox2 appear to have occurred dur ing recent legume evolution, more recently than previously inferred. Many i ntermediate stages of the gene transfer process are represented by cox2 gen es in the studied legumes. Nine legumes contain intact copies of both nucle ar and mt cox2, although transcripts could not be detected for some of thes e genes. Bath cox2 genes are transcribed in seven legumes that are phylogen etically interspersed with species displaying only nuclear or mt cox2 expre ssion. Inactivation of cox2 in each genome has taken place multiple times a nd in a variety of ways, including loss of detectable transcripts or transc ript editing and partial to complete gene loss. Phylogenetic evidence shows about the same number (3-5) of separate inactivations of nuclear and mt co x2, suggesting that there is no selective advantage for a mt vs. nuclear lo cation of cox2 in plants. The current distribution of cox2 presence and exp ression between the nucleus and mitochondrion in the studied legumes is pro bably the result of chance mutations silencing either cox2 gene.