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      Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature

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          Abstract

          Clock-regulated pathways coordinate the response of many developmental processes to changes in photoperiod and temperature. We model two of the best-understood clock output pathways in Arabidopsis, which control key regulators of flowering and elongation growth. In flowering, the model predicted regulatory links from the clock to CYCLING DOF FACTOR 1 ( CDF1) and FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 ( FKF1) transcription. Physical interaction data support these links, which create threefold feed-forward motifs from two clock components to the floral regulator FT. In hypocotyl growth, the model described clock-regulated transcription of PHYTOCHROME-INTERACTING FACTOR 4 and 5 ( PIF4, PIF5), interacting with post-translational regulation of PIF proteins by phytochrome B (phyB) and other light-activated pathways. The model predicted bimodal and end-of-day PIF activity profiles that are observed across hundreds of PIF-regulated target genes. In the response to temperature, warmth-enhanced PIF4 activity explained the observed hypocotyl growth dynamics but additional, temperature-dependent regulators were implicated in the flowering response. Integrating these two pathways with the clock model highlights the molecular mechanisms that coordinate plant development across changing conditions.

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          Most cited references71

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          Structure and function of the feed-forward loop network motif.

          Engineered systems are often built of recurring circuit modules that carry out key functions. Transcription networks that regulate the responses of living cells were recently found to obey similar principles: they contain several biochemical wiring patterns, termed network motifs, which recur throughout the network. One of these motifs is the feed-forward loop (FFL). The FFL, a three-gene pattern, is composed of two input transcription factors, one of which regulates the other, both jointly regulating a target gene. The FFL has eight possible structural types, because each of the three interactions in the FFL can be activating or repressing. Here, we theoretically analyze the functions of these eight structural types. We find that four of the FFL types, termed incoherent FFLs, act as sign-sensitive accelerators: they speed up the response time of the target gene expression following stimulus steps in one direction (e.g., off to on) but not in the other direction (on to off). The other four types, coherent FFLs, act as sign-sensitive delays. We find that some FFL types appear in transcription network databases much more frequently than others. In some cases, the rare FFL types have reduced functionality (responding to only one of their two input stimuli), which may partially explain why they are selected against. Additional features, such as pulse generation and cooperativity, are discussed. This study defines the function of one of the most significant recurring circuit elements in transcription networks.
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            Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses

            Plant growth is coordinately regulated by environmental and hormonal signals. Brassinosteroid (BR) plays essential roles in growth regulation by light and temperature, but the interactions between BR and these environmental signals remain poorly understood at the molecular level. Here, we show that direct interaction between the dark- and heat-activated transcription factor phytochrome-interacting factor4 (PIF4) and the BR-activated transcription factor BZR1 integrates the hormonal and environmental signals. BZR1 and PIF4 interact with each other in vitro and in vivo, bind to nearly two thousand common target genes, and synergistically regulate many of these target genes, including the PRE family HLH factors required for promoting cell elongation. Genetic analysis indicates that BZR1 and PIFs are interdependent in promoting cell elongation in response to BR, darkness, or heat. These results show that the BZR1-PIF4 interaction controls a core transcription network, allowing plant growth co-regulation by the steroid and environmental signals.
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              Targeted destabilization of HY5 during light-regulated development of Arabidopsis.

              Arabidopsis seedlings display contrasting developmental patterns depending on the ambient light. Seedlings grown in the light develop photomorphogenically, characterized by short hypocotyls and expanded green cotyledons. In contrast, seedlings grown in darkness become etiolated, with elongated hypocotyls and dosed cotyledons on an apical hook. Light signals, perceived by multiple photoreceptors and transduced to downstream regulators, dictate the extent of photomorphogenic development in a quantitative manner. Two key downstream components, COP1 and HY5, act antagonistically in regulating seedling development. HY5 is a bZIP transcription factor that binds directly to the promoters of light-inducible genes, promoting their expression and photomorphogenic development. COP1 is a RING-finger protein with WD-40 repeats whose nuclear abundance is negatively regulated by light. COP1 interacts directly with HY5 in the nucleus to regulate its activity negatively. Here we show that the abundance of HY5 is directly correlated with the extent of photomorphogenic development, and that the COP1-HY5 interaction may specifically target HY5 for proteasome-mediated degradation in the nucleus.
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                Author and article information

                Journal
                Mol Syst Biol
                Mol. Syst. Biol
                msb
                Molecular Systems Biology
                BlackWell Publishing Ltd (Oxford, UK )
                1744-4292
                1744-4292
                January 2015
                19 January 2015
                : 11
                : 1
                : 776
                Affiliations
                [1 ]SynthSys and School of Biological Sciences, University of Edinburgh Edinburgh, UK
                [2 ]Department of Biology, University of Washington Seattle, WA, USA
                [3 ]Biosciences, University of Exeter Exeter, UK
                Author notes
                * Corresponding author. Tel: +44 131 651 9083; E-mail: karen.halliday@ 123456ed.ac.uk
                [‡]

                These authors contributed equally to this work

                [†]

                Present address: Laboratory of Systems & Synthetic Biology, Wageningen URWageningen, The Netherlands

                [§]

                Present address: Department of Life Sciences, Ajou UniversitySuwon, South Korea

                [¶]

                Present address: Department of Crop Genetics, John Innes CentreNorwich, UK

                Subject Categories Quantitative Biology & Dynamical Systems; Plant Biology

                Article
                10.15252/msb.20145766
                4332151
                25600997
                b423337c-542d-4d88-a310-a1a479c9263c
                © 2015 The Authors. Published under the terms of the CC BY 4.0 license

                This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 September 2014
                : 21 November 2014
                : 05 December 2014
                Categories
                Articles

                Quantitative & Systems biology
                gene regulatory networks,heat,hypocotyl elongation,photoperiodism,seasonal breeding

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