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      Brassinosteroid, gibberellin, and phytochrome impinge on a common transcription module in Arabidopsis

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          Abstract

          Brassinosteroid (BR) and gibberellin (GA) promote many similar developmental responses in plants; but their relationship remains unclear. Here we show that BR and GA act interdependently through a direct interaction between the BR-activated BZR1 and GA-inactivated DELLA transcription regulators. GA promotion of cell elongation required BR signaling, whereas BR or active BZR1 can suppresssed the GA-deficient dwarf phenotype. DELLAs directly interacted with BZR1 and inhibited BZR1-DNA binding both in vitro and in vivo. Genome-wide analysis defined a BZR1-dependent GA-regulated transcriptome, which is enriched with light-regulated genes and genes involved in cell wall synthesis and photosynthesis/chloroplast. GA promotion of hypocotyl elongation requires both BZR1 and the phytochrome interacting factors (PIFs), as well as their common downstream targets PREs. The results demonstrate that GA releases DELLA-mediated inhibition of BZR1, and that the DELLA-BZR1-PIF4 interaction defines a core transcription module that mediates coordinated growth regulation by GA, BR and light signals.

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          Most cited references37

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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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            Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses.

            Small-molecule hormones govern every aspect of the biology of plants. Many processes, such as growth, are regulated in similar ways by multiple hormones, and recent studies have revealed extensive crosstalk among different hormonal signaling pathways. These results have led to the proposal that a common set of signaling components may integrate inputs from multiple hormones to regulate growth. In this study, we tested this proposal by asking whether different hormones converge on a common set of transcriptional targets in Arabidopsis seedlings. Using publicly available microarray data, we analyzed the transcriptional effects of seven hormones, including abscisic acid, gibberellin, auxin, ethylene, cytokinin, brassinosteroid, and jasmonate. A high-sensitivity analysis revealed a surprisingly low number of common target genes. Instead, different hormones appear to regulate distinct members of protein families. We conclude that there is not a core transcriptional growth-regulatory module in young Arabidopsis seedlings.
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              Coordinated regulation of Arabidopsis thaliana development by light and gibberellins.

              Light and gibberellins (GAs) mediate many essential and partially overlapping plant developmental processes. DELLA proteins are GA-signalling repressors that block GA-induced development. GA induces degradation of DELLA proteins via the ubiquitin/proteasome pathway, but light promotes accumulation of DELLA proteins by reducing GA levels. It was proposed that DELLA proteins restrain plant growth largely through their effect on gene expression. However, the precise mechanism of their function in coordinating GA signalling and gene expression remains unknown. Here we characterize a nuclear protein interaction cascade mediating transduction of GA signals to the activity regulation of a light-responsive transcription factor. In the absence of GA, nuclear-localized DELLA proteins accumulate to higher levels, interact with phytochrome-interacting factor 3 (PIF3, a bHLH-type transcription factor) and prevent PIF3 from binding to its target gene promoters and regulating gene expression, and therefore abrogate PIF3-mediated light control of hypocotyl elongation. In the presence of GA, GID1 proteins (GA receptors) elevate their direct interaction with DELLA proteins in the nucleus, trigger DELLA protein's ubiquitination and proteasome-mediated degradation, and thus release PIF3 from the negative effect of DELLA proteins.
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                Author and article information

                Journal
                100890575
                21417
                Nat Cell Biol
                Nat. Cell Biol.
                Nature cell biology
                1465-7392
                1476-4679
                6 August 2012
                22 July 2012
                August 2012
                24 March 2013
                : 14
                : 8
                : 810-817
                Affiliations
                [1 ]Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
                [2 ]Institute of Molecular Cell Biology, College of Life Science, Hebei Normal University, Shijiazhuang, Hebei, 050016, China
                [3 ]Department of Biology, Duke University, Durham, North Carolina 27708, USA
                Author notes
                [5 ]Correspondence and requests for materials should be addressed to Z-Y.W. ( zywang24@ 123456stanford.edu )
                [4]

                Authors with equal contributions.

                Article
                NIHMS386891
                10.1038/ncb2546
                3606816
                22820377
                93607c06-abc2-409e-8727-d291cc0a5517

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                Cell biology
                Cell biology

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