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

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.

SUBMITTER: Zhao X

PROVIDER: S-EPMC3410867 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Zhao Xin'Ai X Harashima Hirofumi H Dissmeyer Nico N Pusch Stefan S Weimer Annika K AK Bramsiepe Jonathan J Bouyer Daniel D Rademacher Svenja S Nowack Moritz K MK Novak Bela B Sprunck Stefanie S Schnittger Arp A

PLoS genetics 20120802 8

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 ...[more]

PMID: 22879821

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Project description:Experimental studies of the flowering of Arabidopsis thaliana have shown that a large complex gene regulatory network (GRN) is responsible for its regulation. This process has been mathematically modelled with deterministic differential equations by considering the interactions between gene activators and inhibitors (Valentim et al. in PLoS ONE 10(2):e0116973, 2015; van Mourik et al. in BMC Syst Biol 4(1):1, 2010). However, due to complexity of the model, the properties of the network and the roles of the individual genes cannot be deducted from the numerical solution the published work offers. Here, we propose simplifications of the model, based on decoupling of the original GRN to motifs, described with three and two differential equations. A stable solution of the original model is sought by linearisation of the original model which contributes to further investigation of the role of the individual genes to the flowering. Furthermore, we study the role of noise by introducing and investigating two types of stochastic elements into the model. The deterministic and stochastic nonlinear dynamic models of Arabidopsis flowering time are considered by following the deterministic delayed model introduced in Valentim et al. (2015). Steady-state regimes and stability of the deterministic original model are investigated analytically and numerically. By decoupling some concentrations, the system was reduced to emphasise the role played by the transcription factor Suppressor of Overexpression of Constants1 ([Formula: see text]) and the important floral meristem identity genes, Leafy ([Formula: see text]) and Apetala1 ([Formula: see text]). Two-dimensional motifs, based on the dynamics of [Formula: see text] and [Formula: see text], are obtained from the reduced network and parameter ranges ensuring flowering are determined. Their stability analysis shows that [Formula: see text] and [Formula: see text] are regulating each other for flowering, matching experimental findings. New sufficient conditions of mean square stability in the stochastic model are obtained using a stochastic Lyapunov approach. Our numerical simulations demonstrate that the reduced models of Arabidopsis flowering time, describing specific motifs of the GRN, can capture the essential behaviour of the full system and also introduce the conditions of flowering initiation. Additionally, they show that stochastic effects can change the behaviour of the stability region through a stability switch. This study thus contributes to a better understanding of the role of [Formula: see text] and [Formula: see text] in Arabidopsis flowering.

Dataset Information

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

Publications

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

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