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Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells
Tsuneyoshi Kuroiwac, and
aInstitute of Molecular and Cellular Biosciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan; bInstitute of Low Temperature Science, Hokkaido University, Sapporo, Hokkaido 060-0819, Japan; cDepartment of Life Science, College of Science, Rikkyo (St. Paul's) University, Nishiikebukuro, Toshima-ku, Tokyo 171-8501, Japan; and dGraduate School of Horticulture, Chiba University, 648 Matsudo, Matsudo, Chiba 271-8510, Japan
Communicated by Roy H. Doi, University of California, Davis, CA, May 5, 2008
Received for publication January 17, 2008.
Eukaryotic cells arose from an ancient endosymbiotic associationof prokaryotes, with plant cells harboring 3 genomes as theremnants of such evolution. In plant cells, plastid and mitochondrialDNA replication [organelle DNA replication (ODR)] occurs inadvance of the subsequent cell cycles composed of nuclear DNAreplication (NDR) and cell division. However, the mechanismby which replication of these genomes with different originsis coordinated is largely unknown. Here, we show that NDR isregulated by a tetrapyrrole signal in plant cells, which hasbeen suggested as an organelle-to-nucleus retrograde signal.In synchronized cultures of the primitive red alga Cyanidioschyzonmerolae, specific inhibition of A-type cyclin-dependent kinase(CDKA) prevented NDR but not ODR after onset of the cell cycle.In contrast, inhibition of ODR by nalidixic acid also resultedin inhibition of NDR, indicating a strict dependence of NDRon ODR. The requirement of ODR for NDR was bypassed by additionof the tetrapyrrole intermediates protoporphyrin IX (ProtoIX)or Mg-ProtoIX, both of which activated CDKA without inducingODR. This scheme was also observed in cultured tobacco cells(BY-2), where inhibition of ODR by nalidixic acid preventedCDKA activation and NDR, and these inhibitions were circumventedby Mg-ProtoIX without inducing ODR. We thus show that tetrapyrrole-mediatedorganelle–nucleus replicational coupling is an evolutionaryconserved process among plant cells.
Key Words:Cyanidioschyzon merolae retrograde signal tobacco BY-2
Freely available online through the PNAS open access option.
Author contributions: K.T. designed research; Y. Kobayashi performedresearch; Y. Kobayashi and Y. Kanesaki contributed new reagents/analytictools; Y. Kobayashi, A.T., H.K., and T.K. analyzed data; andY. Kobayashi, Y. Kanesaki, and K.T. wrote the paper.