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A general G1/S-phase cell-cycle control module in the flowering plant Arabidopsis thaliana

Xin'Ai Zhao, Hirofumi Harashima, Nico Dissmeyer, Stefan Pusch, Annika K Weimer, Jonathan Bramsiepe, Daniel Bouyer, Svenja Rademacher, Moritz Nowack UGent and Bela Novak, et al. (2012) PLOS GENETICS. 8(8).
abstract
The decision to replicate its DNA is of crucial importance for every cell and, in many organisms, is decisive for the progression through the entire cell cycle. A comparison of animals versus yeast has shown that, although most of the involved cell-cycle regulators are divergent in both clades, they fulfill a similar role and the overall network topology of G1/S regulation is highly conserved. Using germline development as a model system, we identified a regulatory cascade controlling entry into S phase in the flowering plant Arabidopsis thaliana, which, as a member of the Plantae supergroup, is phylogenetically only distantly related to Opisthokonts such as yeast and animals. This module comprises the Arabidopsis homologs of the animal transcription factor E2F, the plant homolog of the animal transcriptional repressor Retinoblastoma (Rb)-related 1 (RBR1), the plant-specific F-box protein F-BOX-LIKE 17 (FBL17), the plant specific cyclin-dependent kinase (CDK) inhibitors KRPs, as well as CDKA; 1, the plant homolog of the yeast and animal Cdc2+/Cdk1 kinases. Our data show that the principle of a double negative wiring of Rb proteins is highly conserved, likely representing a universal mechanism in eukaryotic cell-cycle control. However, this negative feedback of Rb proteins is differently implemented in plants as it is brought about through a quadruple negative regulation centered around the F-box protein FBL17 that mediates the degradation of CDK inhibitors but is itself directly repressed by Rb. Biomathematical simulations and subsequent experimental confirmation of computational predictions revealed that this regulatory circuit can give rise to hysteresis highlighting the here identified dosage sensitivity of CDK inhibitors in this network.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
PROLIFERATION, EXPRESSION, DIVISION, MALE GAMETOGENESIS, POLLEN DEVELOPMENT, RETINOBLASTOMA PROTEIN, GAMETOPHYTE DEVELOPMENT, QUANTITATIVE PCR DATA, INTRINSICALLY UNSTRUCTURED PROTEINS, DEPENDENT KINASE INHIBITORS
journal title
PLOS GENETICS
PLoS Genet.
volume
8
issue
8
article_number
e1002847
pages
14 pages
Web of Science type
Article
Web of Science id
000308529300011
JCR category
GENETICS & HEREDITY
JCR impact factor
8.517 (2012)
JCR rank
12/161 (2012)
JCR quartile
1 (2012)
ISSN
1553-7404
DOI
10.1371/journal.pgen.1002847
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
3035513
handle
http://hdl.handle.net/1854/LU-3035513
date created
2012-10-26 15:27:46
date last changed
2012-10-30 11:37:45
@article{3035513,
  abstract     = {The decision to replicate its DNA is of crucial importance for every cell and, in many organisms, is decisive for the progression through the entire cell cycle. A comparison of animals versus yeast has shown that, although most of the involved cell-cycle regulators are divergent in both clades, they fulfill a similar role and the overall network topology of G1/S regulation is highly conserved. Using germline development as a model system, we identified a regulatory cascade controlling entry into S phase in the flowering plant Arabidopsis thaliana, which, as a member of the Plantae supergroup, is phylogenetically only distantly related to Opisthokonts such as yeast and animals. This module comprises the Arabidopsis homologs of the animal transcription factor E2F, the plant homolog of the animal transcriptional repressor Retinoblastoma (Rb)-related 1 (RBR1), the plant-specific F-box protein F-BOX-LIKE 17 (FBL17), the plant specific cyclin-dependent kinase (CDK) inhibitors KRPs, as well as CDKA; 1, the plant homolog of the yeast and animal Cdc2+/Cdk1 kinases. Our data show that the principle of a double negative wiring of Rb proteins is highly conserved, likely representing a universal mechanism in eukaryotic cell-cycle control. However, this negative feedback of Rb proteins is differently implemented in plants as it is brought about through a quadruple negative regulation centered around the F-box protein FBL17 that mediates the degradation of CDK inhibitors but is itself directly repressed by Rb. Biomathematical simulations and subsequent experimental confirmation of computational predictions revealed that this regulatory circuit can give rise to hysteresis highlighting the here identified dosage sensitivity of CDK inhibitors in this network.},
  articleno    = {e1002847},
  author       = {Zhao, Xin'Ai and Harashima, Hirofumi and Dissmeyer, Nico and Pusch, Stefan and Weimer, Annika K and Bramsiepe, Jonathan and Bouyer, Daniel and Rademacher, Svenja and Nowack, Moritz and Novak, Bela and Sprunck, Stefanie and Schnittger, Arp},
  issn         = {1553-7404},
  journal      = {PLOS GENETICS},
  keyword      = {PROLIFERATION,EXPRESSION,DIVISION,MALE GAMETOGENESIS,POLLEN DEVELOPMENT,RETINOBLASTOMA PROTEIN,GAMETOPHYTE DEVELOPMENT,QUANTITATIVE PCR DATA,INTRINSICALLY UNSTRUCTURED PROTEINS,DEPENDENT KINASE INHIBITORS},
  language     = {eng},
  number       = {8},
  pages        = {14},
  title        = {A general G1/S-phase cell-cycle control module in the flowering plant Arabidopsis thaliana},
  url          = {http://dx.doi.org/10.1371/journal.pgen.1002847},
  volume       = {8},
  year         = {2012},
}

Chicago
Zhao, Xin’Ai, Hirofumi Harashima, Nico Dissmeyer, Stefan Pusch, Annika K Weimer, Jonathan Bramsiepe, Daniel Bouyer, et al. 2012. “A General G1/S-phase Cell-cycle Control Module in the Flowering Plant Arabidopsis Thaliana.” Plos Genetics 8 (8).
APA
Zhao, X., Harashima, H., Dissmeyer, N., Pusch, S., Weimer, A. K., Bramsiepe, J., Bouyer, D., et al. (2012). A general G1/S-phase cell-cycle control module in the flowering plant Arabidopsis thaliana. PLOS GENETICS, 8(8).
Vancouver
1.
Zhao X, Harashima H, Dissmeyer N, Pusch S, Weimer AK, Bramsiepe J, et al. A general G1/S-phase cell-cycle control module in the flowering plant Arabidopsis thaliana. PLOS GENETICS. 2012;8(8).
MLA
Zhao, Xin’Ai, Hirofumi Harashima, Nico Dissmeyer, et al. “A General G1/S-phase Cell-cycle Control Module in the Flowering Plant Arabidopsis Thaliana.” PLOS GENETICS 8.8 (2012): n. pag. Print.