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      TOC1–PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis

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          Abstract

          Arabidopsis adapts to elevated temperature by promoting stem elongation and hyponastic growth through a temperature-responsive transcription factor PIF4. Here we show that the evening-expressed clock component TOC1 interacts with and inactivates PIF4, thereby suppressing thermoresponsive growth in the evening. We find that the expression of PIF4 target genes show circadian rhythms of thermosensitivity, with minimum responsiveness in the evening when TOC1 level is high. Loss of function of TOC1 and its close homologue PRR5 restores thermosensitivity in the evening, whereas TOC1 overexpression causes thermo insensitivity, demonstrating that TOC1 mediates the evening-specific inhibition of thermoresponses. We further show that PIF4 is required for thermoadaptation mediated by moderately elevated temperature. Our results demonstrate that the interaction between TOC1 and PIF4 mediates the circadian gating of thermoresponsive growth, which may serve to increase fitness by matching thermoresponsiveness with the day–night cycles of fluctuating temperature and light conditions.

          Abstract

          The PIF4 transcription factor mediates the response of Arabidopsis seedlings to elevated temperature. Here the authors show that PIF4 interacts with the circadian clock component TOC1 which acts to suppress the PIF4-mediated temperature response in the evening.

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          PIFs: pivotal components in a cellular signaling hub.

          A small subset of basic helix-loop-helix transcription factors called PIFs (phytochrome-interacting factors) act to repress seed germination, promote seedling skotomorphogenesis and promote shade-avoidance through regulated expression of over a thousand genes. Light-activated phytochrome molecules directly reverse these activities by inducing rapid degradation of the PIF proteins. Here, we review recent advances in dissecting this signaling pathway and examine emerging evidence that indicates that other pathways also converge to regulate PIF activity, including the gibberellin pathway, the circadian clock and high temperature. Thus PIFs have broader roles than previously appreciated, functioning as a cellular signaling hub that integrates multiple signals to orchestrate regulation of the transcriptional network that drives multiple facets of downstream morphogenesis. The relative contributions of the individual PIFs to this spectrum of regulatory functions ranges from quantitatively redundant to qualitatively distinct. Copyright © 2010 Elsevier Ltd. All rights reserved.
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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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              High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4.

              Exposure of Arabidopsis plants to high temperature (28 degrees C) results in a dramatic change in plant development. Responses to high temperature include rapid extension of plant axes, leaf hyponasty, and early flowering. These phenotypes parallel plant responses to the threat of vegetational shade and have been shown to involve the hormone auxin. In this work, we demonstrate that high temperature-induced architectural adaptations are mediated through the bHLH transcriptional regulator PHYTOCHROME INTERACTING FACTOR 4 (PIF4). Roles for PIF4 have previously been established in both light and gibberellin (GA) signaling, through interactions with phytochromes and DELLA proteins, respectively. Mutants deficient in PIF4 do not display elongation responses or leaf hyponasty upon transfer to high temperature. High temperature-mediated induction of the auxin-responsive gene IAA29 is also abolished in these plants. An early flowering response to high temperature is maintained in pif4 mutants, suggesting that architectural and flowering responses operate via separate signaling pathways. The role of PIF4 in temperature signaling does not, however, appear to operate through interaction with either phytochrome or DELLA proteins, suggesting the existence of a novel regulatory mechanism. We conclude that PIF4 is an important component of plant high temperature signaling and integrates multiple environmental cues during plant development.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                14 December 2016
                2016
                : 7
                : 13692
                Affiliations
                [1 ]Department of Plant Biology, Carnegie Institution for Science , Stanford, California 94305, USA
                [2 ]Department of Bioenergy Science and Technology, Chonnam National University , Gwangju 61186, Korea
                Author notes
                [*]

                These authors contributed equally to this work

                Article
                ncomms13692
                10.1038/ncomms13692
                5171658
                27966533
                d28fb48d-583b-4a5e-8832-a7c3c763b2cf
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 14 April 2016
                : 25 October 2016
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