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The subgenomes of the plant cell, the nuclear genome, the plastome, and the chondriome are known to interact through various types of coevolving macromolecules. The combination of the organellar genome from one species with the nuclear genome of another species often leads to plants with deleterious phenotypes, demonstrating that plant subgenomes coevolve. The molecular mechanisms behind this nuclear-organellar incompatibility have been elusive, even though the phenomenon is widespread and has been known for >70 years. Here, we show by direct and reverse genetic approaches that the albino phenotype of a flowering plant with the nuclear genome of Atropa belladonna (deadly nightshade) and the plastome of Nicotiana tabacum (tobacco) develops as a result of a defect in RNA editing of a tobacco-specific editing site in the plastid ATPase α-subunit transcript. A plastome-wide analysis of RNA editing in these cytoplasmic hybrids and in plants with a tobacco nucleus and nightshade chloroplasts revealed additional defects in the editing of species-specific editing sites, suggesting that differences in RNA editing patterns in general contribute to the pigment deficiencies observed in interspecific nuclear-plastidial incompatibilities.
INTRODUCTION
The most fundamental step in the evolution of the eukaryotic cell was the endosymbiotic acquisition of organelles. The association of formerly free-living prokaryotes with the host cell was followed by a dramatic reorganization of the genomes of both the host and the symbionts. Among other processes, a substantial part of the genetic information of the prokaryotic endosymbionts was transferred into the nuclear genome (Dyall et al., 2004). Many products of these transferred genes have to be reimported into the organelles, and once there, they interact with organellar gene products. This type of interaction requires tight spatiotemporal and quantitative regulation and leads to coevolution of the interacting compartments (Blier et al., 2001; Herrmann et al., 2003). To date, it has not been clear which interactions are evolutionary conserved and which diverge more rapidly. Are there interactions that are specific to a certain taxon, or are most, if not all, interactions common among most species? A way to study these questions is to determine what happens when organelles are exchanged between species. It is interesting that interspecific organelle exchange often leads to malfunctions in cellular development and differentiation, a phenomenon referred to as nuclear-organellar incompatibility.
The initial...