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      Effect of phyB and phyC loss-of-function mutations on the wheat transcriptome under short and long day photoperiods

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          Abstract

          Background

          Photoperiod signals provide important cues by which plants regulate their growth and development in response to predictable seasonal changes. Phytochromes, a family of red and far-red light receptors, play critical roles in regulating flowering time in response to changing photoperiods. A previous study showed that loss-of-function mutations in either PHYB or PHYC result in large delays in heading time and in the differential regulation of a large number of genes in wheat plants grown in an inductive long day (LD) photoperiod.

          Results

          We found that under non-inductive short-day (SD) photoperiods, phyB-null and phyC-null mutants were taller, had a reduced number of tillers, longer and wider leaves, and headed later than wild-type (WT) plants. The delay in heading between WT and phy mutants was greater in LD than in SD, confirming the importance of PHYB and PHYC in accelerating heading date in LDs. Both mutants flowered earlier in SD than LD, the inverse response to that of WT plants. In both SD and LD photoperiods, PHYB regulated more genes than PHYC. We identified subsets of differentially expressed and alternatively spliced genes that were specifically regulated by PHYB and PHYC in either SD or LD photoperiods, and a smaller set of genes that were regulated in both photoperiods. We found that photoperiod had a contrasting effect on transcript levels of the flowering promoting genes VRN-A1 and PPD-B1 in phyB and phyC mutants compared to the WT.

          Conclusions

          Our study confirms the major role of both PHYB and PHYC in flowering promotion in LD conditions. Transcriptome characterization revealed an unexpected reversion of the wheat LD plants into SD plants in the phyB-null and phyC-null mutants and identified flowering genes showing significant interactions between phytochromes and photoperiod that may be involved in this phenomenon. Our RNA-seq data provides insight into light signaling pathways in inductive and non-inductive photoperiods and a set of candidate genes to dissect the underlying developmental regulatory networks in wheat.

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          Most cited references49

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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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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              Phytochrome structure and signaling mechanisms.

              Phytochromes are a widespread family of red/far-red responsive photoreceptors first discovered in plants, where they constitute one of the three main classes of photomorphogenesis regulators. All phytochromes utilize covalently attached bilin chromophores that enable photoconversion between red-absorbing (P(r)) and far-red-absorbing (P(fr)) forms. Phytochromes are thus photoswitchable photosensors; canonical phytochromes have a conserved N-terminal photosensory core and a C-terminal regulatory region, which typically includes a histidine-kinase-related domain. The discovery of new bacterial and cyanobacterial members of the phytochrome family within the last decade has greatly aided biochemical and structural characterization of this family, with the first crystal structure of a bacteriophytochrome photosensory core appearing in 2005. This structure and other recent biochemical studies have provided exciting new insights into the structure of phytochrome, the photoconversion process that is central to light sensing, and the mechanism of signal transfer by this important family of photoreceptors.
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                Author and article information

                Contributors
                nfkippes@ucdavis.edu
                Carl.VanGessel@colostate.edu
                jrrhamilt@gmail.com
                aniakpinar@gmail.com
                hikmet.budak@icloud.com
                jdubcovsky@ucdavis.edu
                stephen.pearce@colostate.edu
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                29 June 2020
                29 June 2020
                2020
                : 20
                : 297
                Affiliations
                [1 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Department of Plant Sciences, , University of California, ; Davis, CA 95616 USA
                [2 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Current address: Department of Plant Biology, UC Davis Genome Center, , University of California, ; Davis, CA 95616 USA
                [3 ]GRID grid.47894.36, ISNI 0000 0004 1936 8083, Department of Soil and Crop Sciences, , Colorado State University, ; Fort Collins, CO 80523 USA
                [4 ]Montana BioAg Inc., Missoula, MT 59802 USA
                [5 ]GRID grid.413575.1, ISNI 0000 0001 2167 1581, Howard Hughes Medical Institute, ; Chevy Chase, MD 20815 USA
                Author information
                http://orcid.org/0000-0002-1794-7618
                Article
                2506
                10.1186/s12870-020-02506-0
                7325275
                32600268
                9a440fe9-a37f-4ab1-8cf9-ff1631ffdc40
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 8 April 2020
                : 18 June 2020
                Funding
                Funded by: Howard Hughes Medical Institute (US)
                Funded by: FundRef http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;
                Award ID: 2017-67007-25939
                Award Recipient :
                Funded by: TUBITAK
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Plant science & Botany
                wheat,heading date,phytochrome,ft1,ft2,ft3,ppd1,vrn1
                Plant science & Botany
                wheat, heading date, phytochrome, ft1, ft2, ft3, ppd1, vrn1

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