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Science Signaling  27 Jan 2009:
Vol. 2, Issue 55, pp. ec27
DOI: 10.1126/scisignal.255ec27

Because eukaryotic cells are thought to have arisen through endosymbiotic interaction with prokaryotes, eukaryotic cells contain not only a nuclear genome but also organellar genomes in mitochondria and, in the case of plants, plastids. In plants, replication of the nuclear DNA is coordinated with replication of the organellar DNA such that organellar DNA replication precedes nuclear DNA replication and cell division. Tetrapyrrole molecules, which are produced through processes involving both plastids and mitochondria, have been reported to mediate signaling between these organelles and the nucleus to regulate nuclear gene expression of proteins destined for these organelles. Kobayashi et al. found that tetrapyrroles are also involved in coupling completion of organellar DNA replication to activation of the G1 cyclin-dependent kinase CDKA and nuclear DNA replication. By following organellar and nuclear DNA replication in the unicellular red algae Cyanidioschyzon merolae, which has a single mitochondrion and plastid and a cell cycle that can be synchronized with light, the authors found that organellar DNA replication preceded and was required for nuclear DNA replication. When the cells were treated with a CDKA-specific inhibitor or an inhibitor of nuclear DNA polymerase, nuclear DNA replication, but not organellar DNA replication, was blocked. When organellar DNA gyrase was inhibited, both organellar DNA replication and nuclear DNA replication were blocked. Addition of tetrapyrrole intermediates activated CDKA and allowed nuclear DNA replication to proceed in the absence of organellar DNA replication. Inhibition of tetrapyrrole synthesis at a time when organellar DNA replication was just completing prevented nuclear DNA replication. A similar process was observed for tobacco BY-2 cells in culture: Nuclear DNA replication required organellar DNA replication, and this prerequisite could be overcome by the addition of tetrapyrrole intermediates. The authors suggest that tetrapyrroles released from the organelles after DNA replication interact with a—so far unknown—cytoplasmic sensor, and then CDKA is activated, allowing the cells to proceed from G1 to S phase.

Y. Kobayashi, Y. Kanesaki, A. Tanaka, H. Kuroiwa, T. Kuroiwa, K. Tanaka, Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc. Natl. Acad. Sci. U.S.A. 106, 803–807 (2009). [Abstract] [Full Text]

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