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Journal of Virology, April 2007, p. 4177-4185, Vol. 81, No. 8
0022-538X/07/$08.00+0     doi:10.1128/JVI.02103-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

The Nanovirus-Encoded Clink Protein Affects Plant Cell Cycle Regulation through Interaction with the Retinoblastoma-Related Protein ^,

Sébastien Lageix,¹ Olivier Catrice,² Jean-Marc Deragon,^1,3 Bruno Gronenborn,² Thierry Pélissier,^1,* and Bertha Cecilia Ramírez^2,*

CNRS UMR 6547 BIOMOVE, Université Blaise Pascal, 63177 Aubière Cedex,¹ Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette,² LGDP, UMR 5096, Université de Perpignan, 66860 Perpignan Cedex, France³

Received 26 September 2006/ Accepted 24 January 2007

Nanoviruses, multicomponent single-stranded DNA plant viruses, encode a unique cell cycle link protein, Clink, that interacts with retinoblastoma-related proteins (RBR). We have established transgenic Arabidopsis thaliana lines that conditionally express Clink or a Clink variant deficient in RBR binding. By controlled induction of Clink expression, we demonstrated the capacity of the Clink protein to alter RBR function in vivo. We showed that transcription of both S-phase-specific and G₂/M-phase-specific genes was up-regulated depending on the RBR-binding proficiency of Clink. Concomitantly, ploidy levels increased in a substantial fraction of leaf cell nuclei. Also, leaf epidermis cells of transgenic plants producing Clink were smaller and more numerous, indicating additional cell divisions in this tissue. Furthermore, cytogenetic analyses following induction of Clink expression in mature leaves revealed the presence of metaphasic and anaphasic nuclei, clear evidence that Clink-mediated RBR inactivation is sufficient to induce quiescent cells to reenter cell cycle progression and, for at least a fraction of them, to pass through mitosis. Expression of Clink had no effect on genes transcribed by RNA polymerases I and III, suggesting that, in contrast to its mammalian homologue, A. thaliana RBR is not involved in the repression of polymerase I and polymerase III transcription. The results of these in vivo analyses firmly establish Clink as a member of the diverse class of multifunctional cell cycle modulator proteins encoded by small DNA viruses.

Published ahead of print on 31 January 2007.

Supplemental material for this article may be found at http://jvi.asm.org/.

T.P. and B.C.R. contributed equally to this work.

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