Phosphorylation of Retinoblastoma-Related Protein by the Cyclin D/Cyclin-Dependent Kinase Complex Is Activated at the G1/S-Phase Transition in Tobacco

Nakagami, Hirofumi; Kawamura, Kazue; Sugisaka, Keiko; Sekine, Masami; Shinmyo, Atsuhiko

doi:10.1105/tpc.002550

Cited by 157 publications

(156 citation statements)

References 55 publications

(55 reference statements)

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“…Only a few potential substrates for CDKs have been identified in plants. They include a retinoblastoma-related protein (25), a heat-shock transcription factor (48), and an NPK1 mitogenactivated protein kinase kinase kinase. 3 Thus, our findings add a new member to the list of target proteins of plant CDKs.…”

Section: Resultsmentioning

confidence: 99%

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

Araki

Ito

Soyano

et al. 2004

Journal of Biological Chemistry

117

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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 G 1 /S transition in the cell cycle. In plants, this type of Myb protein controls the G 2 /M phase by activating or repressing the transcription of cyclin B genes and a variety of other G 2 /M phasespecific genes. In tobacco, two genes for Myb activators, NtmybA1 and NtmybA2, are transcriptionally controlled and are expressed specifically at the G 2 /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 G 2 /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 G 2 /M and that this phosphorylation removes the inhibitory effect of its C-terminal region, thereby activating NtmybA2 specifically at G 2 /M.In the eukaryotic cell cycle, molecular events occur in a well-defined and reproducible sequence. The periodic activation at the transcriptional level of genes that regulate the cell cycle is fundamental to this process. In animals, transcription of several genes induced at the G 1 /S transition is mainly controlled by the E2F/DP heterodimeric transcription factors (for review, see Ref. 1). E2F-binding sequences are found in promoters from many genes that are transcribed at around the time of G 1 /S transition. Both E2F and DP factors have recently been identified in plants (for review, see Ref.2), and some reports indicate that plant E2F/DP factors play a role at the G 1 /S transition (3, 4). By contrast, different mechanisms for G 2 /M phase-specific transcription have been proposed in plants and animals. In animal cells, G 2 /M phase-specific transcription is mainly regulated by two repressor elements known as cell cycle-dependent elements (CDE) and cell cycle gene homology region (CHR) (for review, see Ref. 5). These elements are found in the promoters of various G 2 /M phase-specific genes, which include cdc25C (6), polo-like kinase (7), aurora A (8), and cyclin B2 (9). Mutation of the CDE and CHR elements allows elevated transcription during G 1 and consequent loss of cell cycle-regulated expression. In plants, G 2 /M phase-specific genes do not contain these rep...

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Section: Resultsmentioning

confidence: 99%

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

Araki

Ito

Soyano

et al. 2004

Journal of Biological Chemistry

117

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“…First, CYCD3 could also act as a mitotic cyclin, boosting G 2 /M kinase activity and hence directly enhancing progress from G 2 into mitosis. Although no association between CYCD and mitotic cyclin-dependent kinase has been detected in plant cell extracts using immunoprecipitation or proteomic approaches (32,33), cyclin-dependent kinase can bind Arabidopsis CYCD4;1 and tobacco CYCD3 in vitro (34,35), and histone H1-directed CYCD3 kinase activity is detected in mitotic tobacco suspension cultured BY-2 cells (36). The evidence for CYCD promotion of the G 2 /M transition is equivocal: Antirrhinum CYCD1, when induced at G 2 /M in synchronized BY-2 cells, indeed increased the rate of progression through mitosis (37), and ectopic expression of CYCD3;1 in Arabidopsis trichomes leads to additional mitoses (15).…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses

Dewitte

Scofield²,

Alcasabas³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

339

352

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Current understanding of the integration of cell division and expansion in the development of plant lateral organs such as leaves is limited. Cell number is established during a mitotic phase, and subsequent growth into a mature organ relies primarily on cell expansion accompanied by endocycles. Here we show that the three Arabidopsis cyclin D3 (CYCD3) genes are expressed in overlapping but distinct patterns in developing lateral organs and the shoot meristem. Triple loss-of-function mutants show that CYCD3 function is essential neither for the mitotic cell cycle nor for morphogenesis. Rather, analysis of mutant and reciprocal overexpression phenotypes shows that CYCD3 function contributes to the control of cell number in developing leaves by regulating the duration of the mitotic phase and timing of the transition to endocycles. Petals, which normally do not endoreduplicate, respond to loss of CYCD3 function with larger cells that initiate endocycles. The phytohormone cytokinin regulates cell division in the shoot meristem and developing leaves and induces CYCD3 expression. Loss of CYCD3 impairs shoot meristem function and leads to reduced cytokinin responses, including the inability to initiate shoots on callus, without affecting endogenous cytokinin levels. We conclude that CYCD3 activity is important for determining cell number in developing lateral organs and the relative contribution of the alternative processes of cell production and cell expansion to overall organ growth, as well as mediating cytokinin effects in apical growth and development.cell division ͉ cyclin D ͉ flowering time ͉ plant development

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“…Subsequently, E2F/DP-dependent transcription of cell cycle genes promotes S phase entry and cell cycle progression. Because of its central role in controlling the transcription of cell cycle genes, RB serves as a convergence point for regulating the cell cycle in response to internal and external mitogenic signals (Nakagami et al, 2002;Stevaux et al, 2002;Cobrinik, 2005;Dimova and Dyson, 2005;Wikenheiser-Brokamp, 2006;Jullien et al, 2008;van den Heuvel and Dyson, 2008;Borghi et al, 2010;Henriques et al, 2010;Johnston et al, 2010;Chen et al, 2011;Gutzat et al, 2011Gutzat et al, , 2012Weimer et al, 2012). Recent studies also provide evidence that RB depletion causes metabolic reprogramming and suggest that the RB pathway in animals exerts part of its effect on cell proliferation through the control of Gln metabolism (Nicolay et al, 2013;Reynolds et al, 2014).…”

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confidence: 97%

Defects in a New Class of Sulfate/Anion Transporter Link Sulfur Acclimation Responses to Intracellular Glutathione Levels and Cell Cycle Control

et al. 2014

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We previously identified a mutation, suppressor of mating type locus3 15-1 (smt15-1), that partially suppresses the cell cycle defects caused by loss of the retinoblastoma tumor suppressor-related protein encoded by the MAT3 gene in Chlamydomonas reinhardtii. smt15-1 single mutants were also found to have a cell cycle defect leading to a small-cell phenotype. SMT15 belongs to a previously uncharacterized subfamily of putative membrane-localized sulfate/anion transporters that contain a sulfate transporter domain and are found in a widely distributed subset of eukaryotes and bacteria. Although we observed that smt15-1 has a defect in acclimation to sulfur-limited growth conditions, sulfur acclimation (sac) mutants, which are more severely defective for acclimation to sulfur limitation, do not have cell cycle defects and cannot suppress mat3. Moreover, we found that smt15-1, but not sac mutants, overaccumulates glutathione. In wild-type cells, glutathione fluctuated during the cell cycle, with highest levels in mid G1 phase and lower levels during S and M phases, while in smt15-1, glutathione levels remained elevated during S and M. In addition to increased total glutathione levels, smt15-1 cells had an increased reduced-to-oxidized glutathione redox ratio throughout the cell cycle. These data suggest a role for SMT15 in maintaining glutathione homeostasis that impacts the cell cycle and sulfur acclimation responses.

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Phosphorylation of Retinoblastoma-Related Protein by the Cyclin D/Cyclin-Dependent Kinase Complex Is Activated at the G1/S-Phase Transition in Tobacco

Cited by 157 publications

References 55 publications

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

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

Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses

Defects in a New Class of Sulfate/Anion Transporter Link Sulfur Acclimation Responses to Intracellular Glutathione Levels and Cell Cycle Control

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