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It has long been understood that specific features of a protein and its corresponding import apparatus dictate the behavior of mitochondrial proteins in their intracellular targeting behavior. In plants, the process by which proteins are directed to organelles has been influenced uniquely by the introduction to the cell of plastids. Parallel functions carried out within the mitochondrion and plastid permit the sharing of proteins and emergence of mechanisms to facilitate dual-targeting of the nuclear-encoded products to both compartments. These include transcriptional and translational variations, relaxation of translation initiation controls and conditional cellular influences. Details of the dual targeting system are emerging from recent studies, and evidence of variation in protein targeting behavior across plant families and across organisms implies that the system itself is in flux. This trend towards multi-targeting enhances protein versatility across eukaryotes – one means of cellular response to developmental or environmental influence.