Transcriptional repression by MYB 3R proteins regulates plant organ growth

Abstract

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.

MYB3Rs, plant homologs of Myb oncoproteins, control cell cycle-regulated transcription and form DREAM-like complexes

“…First, we found the strong tendency of the late cell cycle genes to be downregulated in myb3r1/4 (loss of activators) and upregulated in myb3r1/3/5 (loss of repressors). 9,10 However, there were only small numbers of late cell cycle genes that are affected in both myb3r1/4 and myb3r1/3/5 (Fig. 1A).…”

“…8,9 We have recently shown that the other members of MYB3Rs, MYB3R3 and MYB3R5, in Arabidopsis act as transcriptional repressors. 10 Interestingly, MYB3R1, which has redundant function with MYB3R4 activator, 8 has also overlapping repressive function with MYB3R3/5 repressors. This led to unexpected conclusion that MYB3R1 has a dual role in activating and repressing the late cell cycle genes.…”

“…This led to unexpected conclusion that MYB3R1 has a dual role in activating and repressing the late cell cycle genes. 10 In our recent publication, we proposed that the MYB3R activators and repressors act in coordination rather than in competition, and that repressors are active outside of the G2/M in the cell cycle and in developmental postmitotic states, when the MYB3R activators are inactive. 10 In addition, we showed that MYB3R activators and repressors are present in distinct multiprotein complexes that also contain RBR and specific E2F isoforms.…”

“…10 In our recent publication, we proposed that the MYB3R activators and repressors act in coordination rather than in competition, and that repressors are active outside of the G2/M in the cell cycle and in developmental postmitotic states, when the MYB3R activators are inactive. 10 In addition, we showed that MYB3R activators and repressors are present in distinct multiprotein complexes that also contain RBR and specific E2F isoforms. 10,11 These complexes resemble dREAM (Drosophila RBF, E2F2, and Myb) or MMB (Myb-MuvB) complexes in fly, 12,13 and DREAM (DP, RB-like E2F, and MuvB) complex or LINC (LIN complex) in human, 14,15 raising a possibility that MYB3R complexes are plant version of the evolutionarily conserved Keywords: Arabidopsis, cell cycle, cell division, Myb, multiprotein complex, transcription factor *Correspondence to: Masaki Ito; Email: masakito@agr.nagoya-u.ac.jp complexes that control cell cycle-regulated transcription.…”

“…10,11 These complexes resemble dREAM (Drosophila RBF, E2F2, and Myb) or MMB (Myb-MuvB) complexes in fly, 12,13 and DREAM (DP, RB-like E2F, and MuvB) complex or LINC (LIN complex) in human, 14,15 raising a possibility that MYB3R complexes are plant version of the evolutionarily conserved Keywords: Arabidopsis, cell cycle, cell division, Myb, multiprotein complex, transcription factor *Correspondence to: Masaki Ito; Email: masakito@agr.nagoya-u.ac.jp complexes that control cell cycle-regulated transcription. In this article, we expand our discussion made in our recent publication, 10 especially on our proposed model for molecular mechanisms of transcriptional regulation by MYB3Rs. We also provide further discussion and perspectives on the dREAM/DREAM-like complexes found in Arabidopsis, especially on the plant-specific and conserved natures of these complexes.…”