Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development.

Little is known about the mechanisms that control transcription of the mitochondrial and chloroplastic genomes, and their interplay within plant cells. Here, we describe the positional cloning of the Arabidopsis RUG2 gene, which encodes a protein that is dual-targeted to mitochondria and chloroplasts, and is homologous with the metazoan mitochondrial transcription termination factors (mTERFs). In the loss-of-function rug2 mutants, most organs were pale and showed reduced growth, and the leaves exhibited both green and pale sectors, with the latter containing sparsely packed mesophyll cells. Chloroplast and mitochondrion development were strongly perturbed in the rug2-1 mutant, particularly in pale leaf sectors, in which chloroplasts were abnormally shaped and reduced in number, thereby impairing photoautotrophic growth. As expected from the pleiotropic phenotypes caused by its loss-of-function alleles, the RUG2 gene was ubiquitously expressed. In a microarray analysis of the mitochondrial and chloroplastic genomes, 56 genes were differentially expressed between rug2-1 and the wild type: most mitochondrial genes were downregulated, whereas the majority of the chloroplastic genes were upregulated. Quantitative RT-PCR analyses showed that the rug2-1 mutation specifically increases expression of the RpoTp nuclear gene, which encodes chloroplastic RNA polymerase. Therefore, the RUG2 nuclear gene seems to be crucial for the maintenance of the correct levels of transcripts in the mitochondria and chloroplasts, which is essential for optimized functions of these organelles and proper plant development. Our results highlight the complexity of the functional interaction between these two organelles and the nucleus.