Transcriptional repression by MYB3R proteins regulates plant organ growth

Kosuke Kobayashi, Toshiya Suzuki, Eriko Iwata, Norihito Nakamichi, Takamasa Suzuki, Poyu Chen, Misato Ohtani, Takashi Ishida, Hanako Hosoya, Sabine Mueller, Tuende Leviczky, Aladar Pettko-Szandtner, Zsuzsanna Darula, Akitoshi Iwamoto, Mika Nomoto, Yasuomi Tada, Tetsuya Higashiyama, Taku Demura, John H. Doonan, Marie-Theres Hauser, Keiko Sugimoto, Masaaki Umeda, Zoltan Magyar, Laszlo Boegre, Masaki Ito

In multicellular organisms, temporal and spatial regulation of cell proliferation is central for generating organs with defined sizes and morphologies. For establishing and maintaining the postmitotic quiescent state during cell differentiation, it is important to repress genes with mitotic functions. We found that three of the Arabidopsis MYB3R transcription factors synergistically maintain G2/M-specific genes repressed in post-mitotic cells and restrict the time window of mitotic gene expression in proliferating cells. The combined mutants of the three repressor-type MYB3R genes displayed long roots, enlarged leaves, embryos, and seeds. Genome-wide chromatin immunoprecipitation revealed that MYB3R3 binds to the promoters of G2/M-specific genes and to E2F target genes. MYB3R3 associates with the repressor-type E2F, E2FC, and the RETINOBLASTOMA RELATED proteins. In contrast, the activator MYB3R4 was in complex with E2FB in proliferating cells. With mass spectrometry and pairwise interaction assays, we identified some of the other conserved components of the multiprotein complexes, known as DREAM/dREAM in human and flies. In plants, these repressor complexes are important for periodic expression during cell cycle and to establish a post-mitotic quiescent state determining organ size.