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      Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmodulin‐binding transcription activators (CAMTAs) to produce specific gene expression responses

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          Summary

          • Experimental data show that Arabidopsis thaliana is able to decode different calcium signatures to produce specific gene expression responses. It is also known that calmodulin‐binding transcription activators ( CAMTAs) have calmodulin (CaM)‐binding domains. Therefore, the gene expression responses regulated by CAMTAs respond to calcium signals. However, little is known about how different calcium signatures are decoded by CAMTAs to produce specific gene expression responses.

          • A dynamic model of Ca 2+–CaM– CAMTA binding and gene expression responses is developed following thermodynamic and kinetic principles. The model is parameterized using experimental data. Then it is used to analyse how different calcium signatures are decoded by CAMTAs to produce specific gene expression responses.

          • Modelling analysis reveals that: calcium signals in the form of cytosolic calcium concentration elevations are nonlinearly amplified by binding of Ca 2+, CaM and CAMTAs; amplification of Ca 2+ signals enables calcium signatures to be decoded to give specific CAMTA‐regulated gene expression responses; gene expression responses to a calcium signature depend upon its history and accumulate all the information during the lifetime of the calcium signature.

          • Information flow from calcium signatures to CAMTA‐regulated gene expression responses has been established by combining experimental data with mathematical modelling.

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          Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression.

          Abiotic and biotic stresses are major limiting factors of crop yields and cause billions of dollars of losses annually around the world. It is hoped that understanding at the molecular level how plants respond to adverse conditions and adapt to a changing environment will help in developing plants that can better cope with stresses. Acquisition of stress tolerance requires orchestration of a multitude of biochemical and physiological changes, and most of these depend on changes in gene expression. Research during the last two decades has established that different stresses cause signal-specific changes in cellular Ca(2+) level, which functions as a messenger in modulating diverse physiological processes that are important for stress adaptation. In recent years, many Ca(2+) and Ca(2+)/calmodulin (CaM) binding transcription factors (TFs) have been identified in plants. Functional analyses of some of these TFs indicate that they play key roles in stress signaling pathways. Here, we review recent progress in this area with emphasis on the roles of Ca(2+)- and Ca(2+)/CaM-regulated transcription in stress responses. We will discuss emerging paradigms in the field, highlight the areas that need further investigation, and present some promising novel high-throughput tools to address Ca(2+)-regulated transcriptional networks.
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            Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance.

            The Arabidopsis thaliana CBF cold response pathway plays a central role in cold acclimation. It is characterized by rapid cold induction of genes encoding the CBF1-3 transcription factors, followed by expression of the CBF gene regulon, which imparts freezing tolerance. Our goal was to further the understanding of the cis-acting elements and trans-acting factors involved in expression of CBF2. We identified seven conserved DNA motifs (CM), CM1 to 7, that are present in the promoters of CBF2 and another rapidly cold-induced gene encoding a transcription factor, ZAT12. The results presented indicate that in the CBF2 promoter, CM4 and CM6 have negative regulatory activity and that CM2 has both negative and positive activity. A Myc binding site in the CBF2 promoter was also found to have positive regulatory effects. Moreover, our results indicate that members of the calmodulin binding transcription activator (CAMTA) family of transcription factors bind to the CM2 motif, that CAMTA3 is a positive regulator of CBF2 expression, and that double camta1 camta3 mutant plants are impaired in freezing tolerance. These results establish a role for CAMTA proteins in cold acclimation and provide a possible point of integrating low-temperature calcium and calmodulin signaling with cold-regulated gene expression.
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              Shaping the calcium signature.

              In numerous plant signal transduction pathways, Ca2+ is a versatile second messenger which controls the activation of many downstream actions in response to various stimuli. There is strong evidence to indicate that information encoded within these stimulus-induced Ca2+ oscillations can provide signalling specificity. Such Ca2+ signals, or 'Ca2+ signatures', are generated in the cytosol, and in noncytosolic locations including the nucleus and chloroplast, through the coordinated action of Ca2+ influx and efflux pathways. An increased understanding of the functions and regulation of these various Ca2+ transporters has improved our appreciation of the role these transporters play in specifically shaping the Ca2+ signatures. Here we review the evidence which indicates that Ca2+ channel, Ca2+-ATPase and Ca2+ exchanger isoforms can indeed modulate specific Ca2+ signatures in response to an individual signal.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                27 April 2015
                October 2015
                : 208
                : 1 ( doiID: 10.1111/nph.2015.208.issue-1 )
                : 174-187
                Affiliations
                [ 1 ] School of Biological and Biomedical Sciences Durham Centre for Crop Improvement TechnologyDurham University South Road Durham DH1 3LEUK
                [ 2 ] Cell Signalling GroupCancer Research UK Manchester Institute The University of Manchester Manchester M20 4BXUK
                Author notes
                [*] [* ] Authors for correspondence:

                Junli Liu

                Tel: +44 191 3341376

                Email: Junli.liu@ 123456durham.ac.uk

                Marc R. Knight

                Tel: +44 191 334 1224

                Email: M.R.Knight@ 123456durham.ac.uk

                Article
                NPH13428 2015-19066
                10.1111/nph.13428
                4832281
                25917109
                d5cbbb68-ed2b-4350-9fd2-e35a06c150d8
                © 2015 The Authors. New Phytologist © 2015 New Phytologist Trust

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

                History
                : 16 January 2015
                : 26 March 2015
                Page count
                Pages: 14
                Funding
                Funded by: Research Councils UK
                Funded by: Biotechnology & Biological Sciences Research Council
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph13428
                October 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.8.6 mode:remove_FC converted:22.04.2016

                Plant science & Botany
                arabidopsis,calcium signatures,calmodulin (cam),calmodulin‐binding transcription activators (camtas),gene expression,mathematical modelling

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