Regulation of Plastid Gene Expression in the Chloroplast-to-Chromoplast Transition

Plastid biogenesis and differentiation requires coordinated expression of genes encoded in the nuclear and plastid genomes. Knowledge about the regulation of expression in the plastid genome (or plastome) is central to improving our understanding of these processes (reviewed in López-Juez, 2007). The conversion of chloroplasts into carotenoid-accumulating chromoplasts is a hallmark of tomato fruit ripening and an excellent system for the study of plastid differentiation. In chloroplasts, much of the regulation appears to occur at the posttranscriptional level (reviewed in Choquet and Wollman, 2002). Regulation of gene expression during the development of non-green plastids is less well understood.

Kahlau and Bock (pages 856–874) created a microarray representing the tomato plastome to explore the developmental regulation of plastid gene expression. They found that transcript levels for most genes were much lower in green tomato fruits than in leaves but were not further changed during fruit ripening. For most genes, the amount of transcript associated with polysomes (representing active translation) was also drastically lower in fruits than in leaves. In contrast with mRNA levels, which remained steady, mRNA translation continued to decrease throughout fruit ripening. Together, these results suggest that there is regulation of chloroplast transcript accumulation upon the initiation of the fruit developmental program but that translational regulation is the key component of the subsequent chloroplast-to-chromoplast transition.

The exceptions to these global patterns of downregulation were a small number of genes involved in gene expression and one other protein-coding gene, accD, which is the only plastid gene involved in fatty acid synthesis (see figure). Therefore, it appears that chromoplasts retain minimal expression activity to allow the synthesis of the fatty acids needed for carotenoid accumulation.

Figure 1.

Chromoplast gene expression largely serves the production of a single protein. Most plastid genes were strongly downregulated during tomato fruit ripening, similar to the data shown for the photosynthetic gene psbD. By contrast, amounts of accD transcripts, encoding a subunit of acetyl-CoA carboxylase, increase during ripening. Panels show blots of RNA from leaves and ripening fruit probed with psbD (left) and accD (right), with loading controls shown below.

Kahlau and Bock also investigated developmental regulation of the chloroplast and chromoplast transcription and RNA processing systems and show that certain genes exhibit specific developmental patterns with respect to plastid RNA polymerase activities, intron splicing, and RNA editing. Therefore, the reduced translation seen throughout fruit ripening is likely to be achieved via different mechanisms for different genes.

This work provides valuable information about the global patterns of plastome gene expression in tomato fruit. It also illustrates the importance of studying these processes in a variety of tissues and plastid types.