Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

PNAS 106 (3): 803-807

Copyright © 2009 by the National Academy of Sciences.


Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells

Yuki Kobayashia, Yu Kanesakia, Ayumi Tanakab, Haruko Kuroiwac, Tsuneyoshi Kuroiwac, and Kan Tanakaa,d,1

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.

Abstract: Eukaryotic cells arose from an ancient endosymbiotic association of prokaryotes, with plant cells harboring 3 genomes as the remnants of such evolution. In plant cells, plastid and mitochondrial DNA replication [organelle DNA replication (ODR)] occurs in advance of the subsequent cell cycles composed of nuclear DNA replication (NDR) and cell division. However, the mechanism by which replication of these genomes with different origins is coordinated is largely unknown. Here, we show that NDR is regulated by a tetrapyrrole signal in plant cells, which has been suggested as an organelle-to-nucleus retrograde signal. In synchronized cultures of the primitive red alga Cyanidioschyzon merolae, 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 resulted in inhibition of NDR, indicating a strict dependence of NDR on ODR. The requirement of ODR for NDR was bypassed by addition of the tetrapyrrole intermediates protoporphyrin IX (ProtoIX) or Mg-ProtoIX, both of which activated CDKA without inducing ODR. This scheme was also observed in cultured tobacco cells (BY-2), where inhibition of ODR by nalidixic acid prevented CDKA activation and NDR, and these inhibitions were circumvented by Mg-ProtoIX without inducing ODR. We thus show that tetrapyrrole-mediated organelle–nucleus replicational coupling is an evolutionary conserved 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 performed research; Y. Kobayashi and Y. Kanesaki contributed new reagents/analytic tools; Y. Kobayashi, A.T., H.K., and T.K. analyzed data; and Y. Kobayashi, Y. Kanesaki, and K.T. wrote the paper.

The authors declare no conflict of interest.

This article contains supporting information online at

1To whom correspondence should be addressed. E-mail: kntanaka{at}

© 2009 by The National Academy of Sciences of the USA

Arabidopsis ANGULATA10 is required for thylakoid biogenesis and mesophyll development.
R. Casanova-Saez, E. Mateo-Bonmati, S. Kangasjarvi, H. Candela, and J. L. Micol (2014)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Localization and Phylogenetic Analysis of Enzymes Related to Organellar Genome Replication in the Unicellular Rhodophyte Cyanidioschyzon merolae.
T. Moriyama, N. Tajima, K. Sekine, and N. Sato (2014)
Genome Biol Evol 6, 228-237
   Abstract »    Full Text »    PDF »
The kinesin-like protein TOP promotes Aurora localisation and induces mitochondrial, chloroplast and nuclear division.
Y. Yoshida, T. Fujiwara, Y. Imoto, M. Yoshida, M. Ohnuma, S. Hirooka, O. Misumi, H. Kuroiwa, S. Kato, S. Matsunaga, et al. (2013)
J. Cell Sci. 126, 2392-2400
   Abstract »    Full Text »    PDF »
Coordination of Plastid and Light Signaling Pathways upon Development of Arabidopsis Leaves under Various Photoperiods.
A. Lepisto and E. Rintamaki (2012)
Mol Plant 5, 799-816
   Abstract »    Full Text »    PDF »
Interplay between HEAT SHOCK PROTEIN 90 and HY5 Controls PhANG Expression in Response to the GUN5 Plastid Signal.
P. Kindgren, L. Noren, J. d. D. Barajas Lopez, J. Shaikhali, and A. Strand (2012)
Mol Plant 5, 901-913
   Abstract »    Full Text »    PDF »
External Light Conditions and Internal Cell Cycle Phases Coordinate Accumulation of Chloroplast and Mitochondrial Transcripts in the Red Alga Cyanidioschyzon merolae.
Y. Kanesaki, S. Imamura, A. Minoda, and K. Tanaka (2012)
DNA Res 19, 289-303
   Abstract »    Full Text »    PDF »
Plastids Are Major Regulators of Light Signaling in Arabidopsis.
M. E. Ruckle, L. D. Burgoon, L. A. Lawrence, C. A. Sinkler, and R. M. Larkin (2012)
Plant Physiology 159, 366-390
   Abstract »    Full Text »    PDF »
SD3, an Arabidopsis thaliana Homolog of TIM21, Affects Intracellular ATP Levels and Seedling Development.
H. Hamasaki, T. Yoshizumi, N. Takahashi, M. Higuchi, T. Kuromori, Y. Imura, H. Shimada, and M. Matsui (2012)
Mol Plant 5, 461-471
   Abstract »    Full Text »    PDF »
Overproduction of Chl b Retards Senescence Through Transcriptional Reprogramming in Arabidopsis.
Y. Sakuraba, S. Balazadeh, R. Tanaka, B. Mueller-Roeber, and A. Tanaka (2012)
Plant Cell Physiol. 53, 505-517
   Abstract »    Full Text »    PDF »
Plastid-to-Nucleus Retrograde Signals Are Essential for the Expression of Nuclear Starch Biosynthesis Genes during Amyloplast Differentiation in Tobacco BY-2 Cultured Cells.
K. Enami, T. Ozawa, N. Motohashi, M. Nakamura, K. Tanaka, and M. Hanaoka (2011)
Plant Physiology 157, 518-530
   Abstract »    Full Text »    PDF »
The cell cycle, including the mitotic cycle and organelle division cycles, as revealed by cytological observations.
Y. Imoto, Y. Yoshida, F. Yagisawa, H. Kuroiwa, and T. Kuroiwa (2011)
Microscopy (Tokyo) 60, S117-S136
   Abstract »    Full Text »    PDF »
Algal models in plant biology.
J. M. Cock and S. M. Coelho (2011)
J. Exp. Bot. 62, 2425-2430
   Full Text »    PDF »
GUN4-Porphyrin Complexes Bind the ChlH/GUN5 Subunit of Mg-Chelatase and Promote Chlorophyll Biosynthesis in Arabidopsis.
N. D. Adhikari, J. E. Froehlich, D. D. Strand, S. M. Buck, D. M. Kramer, and R. M. Larkin (2011)
PLANT CELL 23, 1449-1467
   Abstract »    Full Text »    PDF »
Hemin and Magnesium-Protoporphyrin IX Induce Global Changes in Gene Expression in Chlamydomonas reinhardtii.
B. Voss, L. Meinecke, T. Kurz, S. Al-Babili, C. F. Beck, and W. R. Hess (2011)
Plant Physiology 155, 892-905
   Abstract »    Full Text »    PDF »
Signaling Events Leading to Red-Light-Induced Suppression of Photomorphogenesis in Wheat (Triticum aestivum).
V. Gupta, A. Roy, and B. C. Tripathy (2010)
Plant Cell Physiol. 51, 1788-1799
   Abstract »    Full Text »    PDF »
Characterization of cell-cycle-driven and light-driven gene expression in a synchronous culture system in the unicellular rhodophyte Cyanidioschyzon merolae.
T. Moriyama, K. Terasawa, K. Sekine, M. Toyoshima, M. Koike, M. Fujiwara, and N. Sato (2010)
Microbiology 156, 1730-1737
   Abstract »    Full Text »    PDF »
Nitrate Assimilatory Genes and Their Transcriptional Regulation in a Unicellular Red Alga Cyanidioschyzon merolae: Genetic Evidence for Nitrite Reduction by a Sulfite Reductase-Like Enzyme.
S. Imamura, M. Terashita, M. Ohnuma, S. Maruyama, A. Minoda, A. P. M. Weber, T. Inouye, Y. Sekine, Y. Fujita, T. Omata, et al. (2010)
Plant Cell Physiol. 51, 707-717
   Abstract »    Full Text »    PDF »
Chloroplast Proteomics and the Compartmentation of Plastidial Isoprenoid Biosynthetic Pathways.
J. Joyard, M. Ferro, C. Masselon, D. Seigneurin-Berny, D. Salvi, J. Garin, and N. Rolland (2009)
Mol Plant
   Abstract »    Full Text »    PDF »
Photosynthetic Research in Plant Science.
A. Tanaka and A. Makino (2009)
Plant Cell Physiol. 50, 681-683
   Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882