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A tetrapyrrole-regulated ubiquitin ligase controls algal nuclear DNA replication

Nature Cell Biology volume 13, pages 483–487 (2011)Cite this article

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Abstract

In plant cells, organelle DNA replication (ODR) is coordinated with nuclear DNA replication (NDR), with ODR preceding NDR during cell cycle progression. We previously showed that the occurrence of ODR is signalled by a tetrapyrrole compound, most likely Mg-protoporphyrin IX (Mg-ProtoIX), resulting in the activation of cyclin-dependent kinase A (CDKA) and consequent initiation of NDR (refs 1, 2, 3). Here we identify an F-box protein of SCF-type E3 ubiquitin ligase (Fbx3) in the red alga Cyanidioschyzon merolae, which inhibits CDKA by ubiquitylating the relevant cyclin and inducing its degradation. Mg-ProtoIX binds to Fbx3 and inhibits cyclin ubiquitylation. Thus, these observations indicate that Fbx3 serves as the receptor for the plastid-to-nucleus retrograde signal Mg-ProtoIX and thereby contributes to a checkpoint mechanism ensuring coordination of ODR and NDR.

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Figure 1: Role of ubiquitin and proteasome-dependent protein degradation in NDR.
Figure 2: Interaction of Fbx proteins with Cyclin 1 and tetrapyrroles.
Figure 3: Effects of tetrapyrroles on the Fbx3–Cyclin 1 interaction.
Figure 4: Analysis of an Fbx3-null mutant.
Figure 5: Model for Mg-ProtoIX signalling in C. merolae.

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References

  1. Kobayashi, Y. et al. Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc. Natl Acad. Sci. USA 106, 803–807 (2009).

    Article  CAS  Google Scholar 

  2. Kanesaki, Y., Kobayashi, Y., Hanaoka, M. & Tanaka, K. Mg-protoporphyrin IX signaling in Cyanidioschyzon merolae. Plant Signal. Behav. 4, 85–88 (2009).

    Article  Google Scholar 

  3. Gough, N. R. Wait for me. Sci. Signal. 2, ec27 (2009).

    Google Scholar 

  4. Leister, D. Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354, 110–116 (2005).

    Article  CAS  Google Scholar 

  5. Kuroiwa, T. The primitive red algae: Cyanidium caldarium and Cyanidioschyzon merolae as model system for investigating the dividing apparatus of mitochondria and plastids. Bioessays 20, 344–354 (1998).

    Article  Google Scholar 

  6. Matsuzaki, M. et al. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428, 653–657 (2004).

    Article  CAS  Google Scholar 

  7. Ohta, N. et al. Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 10, 67–77 (2003).

    Article  CAS  Google Scholar 

  8. Ohta, N., Sato, N. & Kuroiwa, T. Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res. 26, 5190–5198 (1998).

    Article  CAS  Google Scholar 

  9. Nozaki, H. et al. A 100%-complete sequence reveals unusually simple genomic features in the hot spring red alga Cyanidioschyzon merolae. BMC Biol. 5, 28 (2007).

    Article  Google Scholar 

  10. Jung, T., Catalgol, B. & Grune, T. The proteasomal system. Mol. Aspects Med. 30, 191–296 (2009).

    Article  CAS  Google Scholar 

  11. Reed, S. I. The ubiquitin proteasome pathway in cell cycle control. Results Probl. Cell Differ. 42, 147–181 (2006).

    CAS  Google Scholar 

  12. Somers, D. E. & Fujiwara, S. Thinking outside the F-box: novel ligands for novel receptors. Trends Plant Sci. 14, 206 (2009).

    Article  CAS  Google Scholar 

  13. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).

    Article  CAS  Google Scholar 

  14. Kepinski, S. & Leyser, O. The Arabidopsis F-box TIR1 is an auxin receptor. Nature 435, 446–451 (2005).

    Article  CAS  Google Scholar 

  15. Salahudeen, A. A. et al. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326, 722–726 (2009).

    Article  CAS  Google Scholar 

  16. Vashisht, A. A. et al. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 326, 718–721 (2009).

    Article  CAS  Google Scholar 

  17. Ho, M. S., Ou, C., Chan, Y. R., Chien, C. T. & Pi, H. The utility F-box for protein destruction. Cell Mol. Life Sci. 65, 1977–2000 (2008).

    Article  CAS  Google Scholar 

  18. Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 36, D281–D288 (2008).

    Article  CAS  Google Scholar 

  19. Ariyoshi, M. & Schwabe, J. W. A conserved structural motif reveals the essential transcriptional repression function of Spen proteins and their role in developmental signaling. Genes Dev. 17, 1909–1920 (2003).

    Article  CAS  Google Scholar 

  20. Itoh, R., Takahashi, H., Toda, K., Kuroiwa, H. & Kuroiwa, T. DNA gyrase involvement in chloroplast nucleoid division in Cyanidioschyzon merolae. Eur. J. Cell Biol. 73, 252–258 (1997).

    CAS  PubMed  Google Scholar 

  21. Owusu-Ansah, E., Yavari, A., Mandal, S. & Banerjee, U. Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat. Genet. 40, 356–361 (2008).

    Article  CAS  Google Scholar 

  22. Mandal, S., Guptan, P., Ownsu-Ansah, E. & Banerjee, U. Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev. Cell 9, 843–854 (2005).

    Article  CAS  Google Scholar 

  23. Finkel, T. & Hwang, P. M. The Krebs cycle meets the cell cycle: mitochondria and the G1-S transition. Proc. Natl Acad. Sci. USA 106, 11825–11826 (2009).

    Article  CAS  Google Scholar 

  24. Nott, A., Jung, H., Koussevitzky, S. & Chory, J. Plastid-to-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739–759 (2006).

    Article  CAS  Google Scholar 

  25. Mochizuki, N., Tanaka, R., Tanaka, A., Masuda, T. & Nagatani, A. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 105, 15184–15189 (2008).

    Article  CAS  Google Scholar 

  26. Moulin, M., McCormac, A. C., Terry, M. J. & Smith, A. G. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc. Natl Acad. Sci. USA 105, 15178–15183 (2008).

    Article  CAS  Google Scholar 

  27. Imamura, S., Hanaoka, M. & Tanaka, K. The plant-specific TFIIB-related protein, pBrp, is a general transcription factor for RNA polymerase I. EMBO J. 27, 2317–2327 (2008).

    Article  CAS  Google Scholar 

  28. Imamura, S. et al. 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. Plant Cell Physiol. 51, 707–717 (2010).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank T. Kuroiwa and H. Kuroiwa for help with microscopic analysis. This study was supported by a Grant-in-Aid for Creative Scientific Research (16GS0304) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (to K.T.), a Grant-in-Aid for Scientific Research (B) (21370015) from the Japan Society for the Promotion of Science (JSPS) (to K.T.), COE StartUp Program from Chiba University (to K.T.), and by a Special Coordination Fund for Promoting Science and Technology from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (to M.H.).

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Authors and Affiliations

  1. Graduate School of Horticulture, Chiba University, 648 Matsudo, Matsudo, Chiba 271-8510, Japan

    Yuki Kobayashi, Mitsumasa Hanaoka & Kan Tanaka

  2. Department of Biological Sciences, Faculty of Science and Engineering, Chuo University, 1-13-27 Kasuga, Bunkyo-ku, Tokyo 112-8551, Japan

    Sousuke Imamura

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  1. Yuki Kobayashi
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K.T. designed the research; Y.K., S.I. and M.H. carried out the research; and Y.K., M.H. and K.T. wrote the paper.

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Correspondence to Kan Tanaka.

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Kobayashi, Y., Imamura, S., Hanaoka, M. et al. A tetrapyrrole-regulated ubiquitin ligase controls algal nuclear DNA replication. Nat Cell Biol 13, 483–487 (2011). https://doi.org/10.1038/ncb2203

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