POINT-OF-VIEW Transcription 6:5, 106--111; September-December 2015; © 2015 Taylor & Francis Group, LLC

MYB3Rs, plant homologs of Myb oncoproteins, control cell cycle-regulated transcription and form DREAM-like complexes Kosuke Kobayashi1, Toshiya Suzuki1,2, Eriko Iwata1, Zoltan Magyar3,4, Laszlo B€ogre4, and Masaki Ito1,2,* 1

Graduate School of Bioagricultural Sciences; Nagoya University; Chikusa, Nagoya, Japan; 2JST; CREST; Chikusa, Nagoya, Japan; 3Institute of Plant Biology;

Biological Research Centre; Szeged, Hungary; 4Royal Holloway; University of London; School of Biological Sciences; Egham, Surrey, UK

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lant MYB3R transcription factors, homologous to Myb oncoproteins, regulate the genes expressed at G2 and M phases in the cell cycle. Recent studies showed that MYB3Rs constitute multiprotein complexes that may correspond to animal complexes known as DREAM or dREAM. Discovery of the putative homologous complex in plants uncovered their significant varieties in structure, function, dynamics, and heterogeneity, providing insight into conserved and diversified aspects of cell cycle-regulated gene transcription.

Keywords: Arabidopsis, cell cycle, cell division, Myb, multiprotein complex, transcription factor *Correspondence to: Masaki [email protected]

Ito;

Email:

Submitted: 09/29/2015 Revised: 10/08/2015 Accepted: 10/13/2015 http://dx.doi.org/10.1080/21541264.2015.1109746 106

It is generally believed that oscillated transcription of genes is important for proper progression of the cell cycle. There are generally 2 main waves of gene transcription in the cell cycle, one wave occurs at G1 to S phase, which enables timely expression of genes required for DNA replication, whereas the other takes place later during G2 and M phases and drives entry into and progression through mitosis.1,2 In addition to their transcriptional regulation within the cell cycle, both early and late cell cycle genes need to be expressed in differentiated cells after developmental arrest of cell proliferation. In general, it has been known that the early cell cycle genes are regulated by heterodimeric transcription factors that are composed of E2F and DP family proteins and bind to the E2F motifs located in their promoter regions.3,4 On the other hand, we have shown that, in plants, the late cell cycle genes are regulated by R1R2R3-type Myb transcription factors, also known as MYB3Rs, that bind to the mitosis-specific activator (MSA) elements in target promoters.5,6 This type of Myb transcription factors have domain Transcription

structures similar to animal Myb oncoprotein and is believed to be ancestors of diverged R2R3-Myb genes that are specific to plant lineage.7 Among 5 MYB3R genes in Arabidopsis, MYB3R1 and MYB3R4 were found to be transcriptional activators that regulate late cell cycle genes and have critical roles for executing mitosis and cytokinesis.8 Loss of both genes by mutations resulted in downregulation of a subset of the late cell cycle genes and frequent occurrence of incomplete cytokinesis that is due to decreased expression of the critical target gene, KNOLLE.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.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 Volume 6 Issue 5

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).10 If the members of MYB3R generally act in competition for transcriptional regulation, most of the target genes should be oppositely affected by activators and repressors. However, it is not the case. Second, we could not observe significant effects on gene expression changes upon combined mutations in activator- and repressor-type MYB3Rs Activator and Repressor MYB3Rs: (myb3r1/3/4/5), comparing with mutaCoordination Rather than tions in either type of MYB3Rs (myb3r1/4 Competition or myb3r1/3/5) (Fig. 1A).10 The competitive interaction would predict intermediThere are generally 2 main modes of ate levels of target expression upon action for transcriptional repressors, pascombined loss of activators and repressors. sive repression and active repression.16 However, there are only a few late cell cycle genes behaving in this way.10 Third, the myb3r1/4 and myb3r1/3/5 plants showed distinct cellular abnormalities, which were not recovered by combined mutations in activators and repressors (myb3r1/3/4/5).10 This is in clear contrast to the antagonistic genetic interaction between activator and repressor E2Fs (E2F1 and E2F2) in Drosophila.3 The absence of genetic interaction between MYB3Rs provides evidence against competitive interaction between activators and repressors. All these results make it unlikely that MYB3R repressors may act as passive repressors that interfere with activators. Our current explanation is that MYB3R activators and repressors act in coordination rather than in competition. More precisely, MYB3R activators and repressors may act in different timing within cell cycle and at different stage during organ development, thus avoidFigure 1. MYB3R-midated transcriptional regulation of the late cell cycle genes in Arabidopsis. (A) MYB3R ing competition between activators activators and repressors affect separate subsets of the late cell cycle genes. The microarray data of plants with MYB3R mutant combinations was visualized by heat map, where green and red indicate downregulaand repressors.10,11 This idea tion and upregulation, respectively, in comparison with wild type plants. DAct, mutations in MYB3R activacomes, in part, from our observators (myb3r1/4); DRep, mutations in MYB3R repressors (myb3r1/3/5); and DActRep, mutations in both MYB3R tion of CYCB1;2-YFP expression activators and repressors (myb3r1/3/4/5). (B) MYB3R repressors preferentially impact on the late cell cycle in Arabidopsis, which showed that genes, although MYB3R3 binds to both late cell cycle genes and E2F target genes. Venn diagram shows the loss of MYB3R repressors caused overlap between MYB3R3-bound genes defined by ChIP-seq experiments and the late cell cycle genes or E2F target genes. There are 71 late cell cycle genes and 54 E2F target genes that are also classified as ectopic expression of the target MYB3R3-bound genes (398 genes in total). Their expression signals in microarray data were subjected to gene outside of the G2/M in the scattered plot analysis comparing expression in wild type and DRep plants. cell cycle and after differentiation

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.

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Passive repression is achieved by interfering transcriptional activators through inhibitory protein-protein interaction or competitive binding to DNA with same cis-acting motifs. On the other hand, active repressors have intrinsic repressive capacity, which is usually exerted by the defined repression domains. Activator and repressor MYB3Rs both contain N-terminally located conserved DNA-biding domain, so called Myb domain,7 consistently with the idea of competitive binding of activators and repressors to the MSA motif. However, by following observations, we proposed that activator- and repressor-type MYB3Rs do not compete with each other, but rather act coordinately for regulation of the late cell cycle genes. First, we found the strong tendency of the late cell cycle genes to be

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during organ development.10 This suggests that MYB3R repressors may play their functions when MYB3R4 is not functional due to its repressed expression.8 This explanation is also consistent with the dual function of MYB3R1 acting as both activator and repressor, because it is unlikely that MYB3R1 plays both functions at the same time in the same cells, but is more plausible to assume temporal alternation of MYB3R1 function, switching between activation and repression. Activity of MYB3R activators and repressors may be under opposite temporal regulation in the cell cycle and during development, such that both types of MYB3Rs are not activated simultaneously in the same cells.

MYB3Rs are Always Busy: Activation at G2/M and Repression Outside of G2/M Our genome-wide gene expression data showed that loss of MYB3R activators results in downregulation of a subset of the late cell cycle genes, whereas loss of MYB3R repressors upregulates a separate subset (Fig. 1A). The intriguing questions are why only subset of target genes is sensitive to the loss of MYB3Rs, and why MYB3R activators and repressors affect separate subsets.10 One explanation for this observation is that activators and repressors may act selectively on the nonoverlapping subsets of MYB3R target genes. However, the core MSA sequence in the downregulated and upregulated genes are more or less equivalent,9,10 making it unlikely for MYB3Rs to recognize separate subsets through different DNAbiding preferences. Moreover, our ChIPseq data shows that MYB3R3 repressor associates with the late cell cycle genes, regardless of whether they are affected or not by loss of MYB3R repressors.10 Our preferred hypothesis is that the impact of MYB3R repressors may depend on the contexts of the target promoters. More specifically, when the target promoters have strong basal activities (activities of cis elements other than MSA elements), loss of MYB3R repressors may result in promoter activation due to derepression of the basal activity, whereas such activation

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may not be evident when the basal activities of target promoters are low or negligible. In this hypothesis, MYB3R repressors are assumed to bind and execute their roles equally on essentially all their target genes, but their impacts vary depending on the basal activities of the target promoters. Apparent effect of MYB3R activators may be estimated lower when the target promoters have higher basal activities that mask the actual MYB3Rmedaited activation, whereas it may be underscored for the target genes with low basal promoter activities. This idea predicts that promoter basal activities influence the impact of MYB3R activators and repressors in opposite way, thus explaining non-overlapping subsets affected by loss of activators and repressors (Fig. 1A). Taking all these considerations together, we would like to propose that there may be 2 different modes of regulation to achieve oscillated transcription of late cell cycle genes; one is activation at G2/M that is mediated by MYB3R activators, and the other is repression outside of G2/M that is regulated by MYB3R repressors. The former has strong impact on the genes with weak basal promoter activities, whereas the latter is more important when the basal activities are strong. Most of the late cell cycle genes may have moderate basal activities, and may be intermediately affected by both activation and repression, as actually observed in transcriptome data (Fig. 1A). This idea is also consistent with the above-mentioned potential coordination between activators and repressors, where MYB3R activators and repressors fulfill their roles at G2/M and outside of the G2/M, respectively, without competing with each other by acting in the same cells at the same time. To achieve this temporal alternation, there may a selector mechanism that alternate 2 different cellular statuses: activator-on/repressor-off state and activator-off/repressor-on state. Such regulation may be achieved through a mechanism linking regulation of activators and repressors. We showed previously that the CDK-mediated phosphorylation of the MYB3R activator enhanced its activity for transcriptional activation in tobacco cells.17 This CDK-dependent regulation may provide potential selector mechanism

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if the related CDK activity act oppositely on MYB3R repressors. Alternatively, MYB3R activators and repressors, forming the distinct multiprotein complexes similar to DREAM/dREAM complex in mammals and fly, may be regulated as a whole functional complex.10 Both activator and repressor complexes may have common component proteins, which may provide a target of post-translation regulation that may oppositely influence the activator and repressor complexes.

MYB3Rs Under CDK Regulation: Possible Involvement in Growth Inhibition Under Stress The CDK-mediated phosphorylation of MYB3R activators and their resulting enhanced activity may provide the positive feedback mechanisms, where MYB3Rs activate transcription of mitotic cyclin genes, which, in turn, enhance the activity of MYB3R activators though increased CDK activity.17 We previously proposed that this positive feedback loop may explain the irreversible nature of mitosis in the cell cycle, as we can expect that subtle increase of mitotic CDK activity should activate the feedback loop, thus leading to the burst of mitotic gene expression.17 Here, we expand our argument on the functional interaction between MYB3Rs and CDK beyond the regulation within the cell cycle, and discuss the possibility that it may be also operating for environmental control of plant growth. It is known that various abiotic and biotic stresses inhibit plant growth and that this inhibition involves active repression of cell proliferation.18,19 Under different stress conditions, plants often induce the expression of the negative regulators of cell cycle, such as KRP and SIM/SMR families of CDK inhibitors, which causes reduced activity of CDK and possibly of MYB3R activators as the consequence.20,21 This may lead to decreased amount of mitotic cyclins and other mitotic regulators due to their decreased transcription, which further lead to decreased mitotic CDK activity, thus constituting again feedback loop for stabilization of low CDK activity and inhibited cell cycle under stress. It is also

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noteworthy that stress-induced decrease of gibberellin, a well-known plant hormone with general positive roles in plant growth, may be important for growth inhibition under stress.22 A member of GRAS family transcription factors, known as DELLA, accumulate in the absence of gibberellin and lead to upregulation of SIMI/SMR members,23 and downregulation of cyclins and CDKs with mitotic functions.24 Another plant hormone, abscisic acid, accumulates under water stress condition and induces KRP1 expression.25 Under DNA stress, a NAC domain family transcription factor, SOG1, activates transcription of SMR5 and SMR7,20 and may consequently reduce the CDK activity. Therefore, in various contexts of stressinduced growth inhibition, plants respond commonly by lowering the CDK activity, and the CDK-MYB3R interaction may stabilize such lowered activity of CDK. We would like to propose that interaction between MYB3Rs and CDK may provide the core mechanism for hormonally- and environmentally-induced growth inhibition in plants. It is of interest to explore whether MYB3R repressors, as is the case of activators, are also controlled by CDK-

mediated phosphorylation. In this context, it should be noted that Arabidopsis leaves express at least 2 separate protein complexes containing both MYB3Rs and CDK, MYB3R3 (repressor) and CDKA;1 in one complex and MYB3R4 (activator) and CDKA;1 in the other.10

complex binds either to B-Myb in S phase (forming B-Myb-MuvB complex) or Rbrelated protein p130, E2F4, and DP in G0/G1 (forming DREAM complex) (Fig. 2).14,15 Drosophila also have similar complex, known as dREAM, which contains component proteins that are homologous to those in human DREAM complex.12,13 Mass spectrometry proteomic analysis in Arabidopsis leaves sugMYB3Rs are Not Alone: Acting gested that the MYB3R-containing Together with E2Fs in DREAMcomplex also contains proteins homoloLike Complexes gous to DP, LIN9 (ALY2 or ALY3), and We found that MYB3Rs are present in LIN54 (TCX5), consistently with the idea a complex that also contains E2F isoforms that the complex may be plant version of 10 and RBR in Arabidopsis leaves.10 In ani- dREAM/DREAM complexes. Absence mals, it has been known that Myb func- of the Arabidopsis genes orthologous to tions together with large multiprotein LIN37 and LIN52 may suggest that the complexes, called DREAM or LINC in complexes in plants may have substantial human,14,15 and dREAM or MMB in differences from the conserved dREAM/ Drosophila,12,13 which are critical for tran- DREAM complexes in animals (Fig. 2). scriptional regulation of the early cell cycle To make more conclusive arguments on genes in human, and for late cell cycle the MYB3R-containing complexes in Aragenes in both human and fly .1,11 In bidopsis, we need further precise proteomic human, the complex is constituted by at analysis to identify the rest of component least 8 component proteins, among which proteins and also genetic studies to eluci11 5 proteins (RBBP4, LIN9, LIN37, date their functional interactions. Nevertheless, it would be of interest to LIN52, and LIN54) form a stable core complex called the MuvB core. This core make further speculation on the conserved and divergent properties of MYB3R-contanting complexes, by expanding the hypothesis that they may be evolutionally related to DREAM/dREAM complexes. Most importantly, the plant complexes differ from those in animals in that plants may have 2 distinct complexes containing different pairs of Myb and E2F family proteins.10 One may represent putative activator complex containing MYB3R4 and E2FB, both of which are known as transcriptional activator, whereas the other contains MYB3R3 and E2FC with repression functions, and may act as a repressor complex. In contrast, human complexes can function either as activator Figure 2. Component proteins of human DREAM and B-Myb-MuvB complexes and their homologues in Ara(B-Myb-MuvB complex) or bidopsis. Arabidopsis genome encodes proteins homologous to B-Myb, LIN9, LIN54, RBBP4, E2F4, DP1, and repressor (DREAM complex) p130, but does not contain genes for LIN37 and LIN52. Except for RBR1, the homologous proteins are depending on the composition of encoded by multigene families in Arabidopsis. It should be noted that ALY1, ALY2 and ALY3, homologous to LIN9, have plant-specific N-terminal extension with single Myb domain. Numbers at the bottom of each box the complexes, where B-Myb is represent score and E-value (shown in parentheses) obtained by comparing human and Arabidopsis proteins required for switching the represby Blast program. Shown are the lowest E-values that were recorded among the members in each protein sing complexes into those with family. activation function for the

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transcription of late cell cycle genes.26,27 Drosophila dREAM complex, containing simultaneously both dMyb and E2F2, has both activation and repression functions on the different target genes.13 The dREAM complex represses E2F-target genes with various roles in developmental pathways, whereas it is involved in activation of the late cell cycle genes. Elaborate genetic studies in Drosophila suggested that dMyb, as B-Myb in human, plays a role in switching repressor into activator complexes.27,28 Plants, possessing both activation and repression complexes separately,10 may have different mechanisms to select which complex to be activated depending on the cellular status within the cell cycle and developmental processes. It should be also noted that plants do not have homologs of a forkhead domain transcription factor, FoxM1, which is recruited to the target promoters by BMyb and bind to MuvB core to fulfill its essential function in activation of the late cell cycle genes.26 We also found differences in co-existence of the Myb and the E2F family proteins in the complexes. They coexist in Drosophila and Arabidopsis, at least in the cellular status under applied experimental conditions,10,12,13 unlike human cells in which B-Myb and E2F4 bind to the MuvB core in a temporally-separated manner.26 In Drosophila, genome-wide protein-DNA interaction assay by ChIPseq revealed both E2F2 and dMyb are commonly present in most of the dREAM targets.13 Similarly, MYB3R3 binds to both the late cell cycle genes and E2F target genes in Arabidopsis.10 Importantly, in both systems, functional interaction between Myb and E2F is not evident in target regulation. In Drosophila, RNAimediated depletion of dMyb and E2F2 results in altered expression of mutually exclusive subsets of dREAM targets, those predominantly recognized by dMyb and E2F2, respectively.13 Situations are similar in Arabidopsis, where loss of MYB3Rs affect the late cell cycle genes, but not E2F target genes, in spite that they are bound by MYB3R3 in vivo (Fig. 1B).10 Therefore, one of the most interesting and challenging questions on these conserved multiprotein complexes is why 2 main cell cycle transcriptional regulators, Myb and

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E2F, exist together in the same complex in plants and insects. This issue may be related to the observation that only 25% of genes bound by dREAM/MMB in vivo showed altered expression when the component proteins were depleted by RNAi in Drosophila.13 Considering the evolutional conservation of Myb-E2F coexistence, there should be some biological significance leading to increased fitness, at least, under their living environments. One possibility is that significance of Myb-E2F coexistence may not be apparent in experimental conditions, but evident only under certain biotic or abiotic stresses. Alternatively, its significance may be related to some cellular processes other than gene transcription, such as initiation of DNA replication as suggested in Drosophila.13,29 Finding of complexes containing both Myb and E2F in plants, in addition to fly, would help us to solve this mystery in future.

Disclosure of Potential Conflicts of Interest

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checkpoint in response to reactive oxygen species. Plant Cell 2014; 26:296-309; PMID: 24399300; http://dx. doi.org/10.1105/tpc.113.118943 21. Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A, Vandepoele K, Magyar Z, Hatzfeld Y, Van Der Schueren E, Beemster GT, et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J Biol Chem 2007; 282:25588-96; PMID: 17599908; http://dx.doi.org/ 10.1074/jbc.M703326200 22. Colebrook EH, Thomas SG, Phillips AL, Hedden P. The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 2014; 217:67-75; PMID: 24353205; http://dx.doi.org/10.1242/jeb.089938 23. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P. Gibberellin signaling controls cell proliferation rate in Arabidopsis.

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

Plant MYB3R transcription factors, homologous to Myb oncoproteins, regulate the genes expressed at G2 and M phases in the cell cycle. Recent studies s...
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