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J. Biol. Chem., Vol. 279, Issue 31, 32979-32988, July 30, 2004

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Mitotic Cyclins Stimulate the Activity of c-Myb-like Factors for Transactivation of G₂/M Phase-specific Genes in Tobacco^*

Satoshi Araki, Masaki Ito¶||, Takashi Soyano, Ryuichi Nishihama, and Yasunori Machida

From the Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan and the ^¶Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo 7-3-1, Tokyo 113-0033, Japan

Myb transcription factors, which contain three imperfect repeats in the Myb domain, are evolutionarily conserved members of the Myb superfamily. Vertebrate Myb proteins with three repeats, c-Myb, A-Myb, and BMyb, play important roles at the G₁/S transition in the cell cycle. In plants, this type of Myb protein controls the G₂/M phase by activating or repressing the transcription of cyclin B genes and a variety of other G₂/M phase-specific genes. In tobacco, two genes for Myb activators, NtmybA1 and NtmybA2, are transcriptionally controlled and are expressed specifically at the G₂/M phase. As we showed here, in addition to the control at the transcriptional level, activity of NtmybA2 is also controlled at the post-translational level. We found that the transactivation potential of NtmybA2 is repressed by a regulatory domain located at its carboxyl terminus and that specific classes of cyclins A and B enhanced NtmybA2 activity possibly by relieving this inhibitory effect. Mutations at the 20 potential sites of phosphorylation by cyclin-dependent kinase (CDK) in NtmybA2 blocked the enhancing effects of the cyclins on NtmybA2 activity. Recombinant NtmybA2 was phosphorylated in vitro by a CDK fraction prepared from tobacco BY2 cells. The kinase activity for NtmybA2 in the CDK fraction was cell cycle-regulated in BY2 cells, peaking at the G₂/M phase when the level of transcripts of cyclin B is maximal. Taken together, our data suggest that NtmybA2 is phosphorylated by a specific cyclin/CDK complex(es) at G₂/M and that this phosphorylation removes the inhibitory effect of its C-terminal region, thereby activating NtmybA2 specifically at G₂/M.

Received for publication, March 22, 2004 , and in revised form, May 26, 2004.

^* This work was supported in part by a grant from Program for Promotion of Basic Research Activities for Innovative Biosciences and by Grants-in-Aid 14036216 and 14036211 for Scientific Research on Priority Areas from the Ministry of Education, Science, Culture and Sports of Japan. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Present address: Central Research Institute, Ishihara Sangyo Kaisha, Ltd., Kusatsu, Shiga 525-0025, Japan.

^|| To whom correspondence should be addressed: Department of Regulation of Biological Signals, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. Tel.: 81-52-789-4168; Fax: 81-52-789-4165; E-mail: masakito{at}agr.nagoya-u.ac.jp.

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