A MECHANISM FOR INTERGENOMIC INTEGRATION - ABUNDANCE OF RIBULOSE-BISPHOSPHATE CARBOXYLASE SMALL-SUBUNIT PROTEIN INFLUENCES THE TRANSLATION OF THE LARGE-SUBUNIT MESSENGER-RNA

Multimeric protein complexes in chloroplasts and mitochondria are gene rally composed of products of both nuclear and organelle genes of the cell. A central problem of eukaryotic cell biology is to identify and understand the molecular mechanisms for integrating the production and accumulation of the products of the two separate genomes. Ribulose bi sphosphate carboxylase (Rubisco) is localized in the chloroplasts of p hotosynthetic eukaryotic cells and is composed of small subunits (SS) and large subunits (LS) coded for by nuclear rbcS and chloroplast rbcL genes, respectively. Transgenic tobacco plants containing antisense r bcS DNA have reduced levels of rbcS mRNA, normal levels of rbcL mRNA, and coordinately reduced LS and SS proteins. Our previous experiments indicated that the rate of translation of rbcL mRNA might be reduced i n some antisense plants; direct evidence is presented here. After a sh ort-term pulse there is less labeled LS protein in the transgenic plan ts than in wild-type plants, indicating that LS accumulation is contro lled in the mutants at the translational and/or posttranslational leve ls. Consistent with a primary restriction at translation, fewer rbcL m RNAs are associated with polysomes of normal size and more are free or are associated with only a few ribosomes in the antisense plants. Eff ects of the rbcS antisense mutation on mRNA and protein accumulation, as well as on the distribution of mRNAs on polysomes, appear to be min imal for other chloroplast and nuclear photosynthetic genes. Our resul ts suggest that SS protein abundance specifically contributes to the r egulation of LS protein accumulation at the level of rbcL translation initiation.