External Light Conditions and Internal Cell Cycle Phases Coordinate Accumulation of Chloroplast and Mitochondrial Transcripts in the Red Alga Cyanidioschyzon merolae

The mitochondria and chloroplasts in plant cells are originated from bacterial endosymbioses, and they still replicate their own genome and divide in a similar manner as their ancestors did. It is thus likely that the organelle transcription is coordinated with its proliferation cycle. However, this possibility has not extensively been explored to date, because in most plant cells there are many mitochondria and chloroplasts that proliferate asynchronously. It is generally believed that the gene transfer from the organellar to nuclear genome has enabled nuclear control of the organelle functions during the evolution of eukaryotic plant cells. Nevertheless, no significant relationship has been reported between the organelle transcriptome and the host cell cycle even in Chlamydomonas reinhardtii. While the organelle proliferation cycle is not coordinated with the cell cycle in vascular plants, in the unicellular red alga Cyanidioschyzon merolae that contains only one mitochondrion, one chloroplast, and one nucleus per cell, each of the organelles is known to proliferate at a specific phase of the cell cycle. Here, we show that the expression of most of the organelle genes is highly coordinated with the cell cycle phases as well as with light regimes in clustering analyses. In addition, a strong correlation was observed between the gene expression profiles in the mitochondrion and chloroplast, resulting in the identification of a network of functionally related genes that are co-expressed during organelle proliferation.