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      Histone H3 lysine 36 methylation affects temperature-induced alternative splicing and flowering in plants

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          Abstract

          Background

          Global warming severely affects flowering time and reproductive success of plants. Alternative splicing of pre-messenger RNA (mRNA) is an important mechanism underlying ambient temperature-controlled responses in plants, yet its regulation is poorly understood. An increase in temperature promotes changes in plant morphology as well as the transition from the vegetative to the reproductive phase in Arabidopsis thaliana via changes in splicing of key regulatory genes. Here we investigate whether a particular histone modification affects ambient temperature-induced alternative splicing and flowering time.

          Results

          We use a genome-wide approach and perform RNA-sequencing (RNA-seq) analyses and histone H3 lysine 36 tri-methylation (H3K36me3) chromatin immunoprecipitation sequencing (ChIP-seq) in plants exposed to different ambient temperatures. Analysis and comparison of these datasets reveal that temperature-induced differentially spliced genes are enriched in H3K36me3. Moreover, we find that reduction of H3K36me3 deposition causes alteration in temperature-induced alternative splicing. We also show that plants with mutations in H3K36me3 writers, eraser, or readers have altered high ambient temperature-induced flowering.

          Conclusions

          Our results show a key role for the histone mark H3K36me3 in splicing regulation and plant plasticity to fluctuating ambient temperature. Our findings open new perspectives for the breeding of crops that can better cope with environmental changes due to climate change.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13059-017-1235-x) contains supplementary material, which is available to authorized users.

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          Most cited references 47

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          A genomic view of alternative splicing.

          Recent genome-wide analyses of alternative splicing indicate that 40-60% of human genes have alternative splice forms, suggesting that alternative splicing is one of the most significant components of the functional complexity of the human genome. Here we review these recent results from bioinformatics studies, assess their reliability and consider the impact of alternative splicing on biological functions. Although the 'big picture' of alternative splicing that is emerging from genomics is exciting, there are many challenges. High-throughput experimental verification of alternative splice forms, functional characterization, and regulation of alternative splicing are key directions for research. We recommend a community-based effort to discover and characterize alternative splice forms comprehensively throughout the human genome.
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            Phytochromes function as thermosensors in Arabidopsis.

            Plants are responsive to temperature, and some species can distinguish differences of 1°C. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). However, the mechanisms of temperature perception are largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm-temperature response, and consistent with this, we show in this background that the warm-temperature transcriptome becomes derepressed at low temperatures. We found that phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature-dependent manner. The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers that integrate temperature information over the course of the night.
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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

                Contributors
                richard.immink@wur.nl
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1474-7596
                1474-760X
                1 June 2017
                1 June 2017
                2017
                : 18
                Affiliations
                [1 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Laboratory of Molecular Biology, , Wageningen University and Research, ; 6708 PB Wageningen, The Netherlands
                [2 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, , Bioscience, Wageningen University and Research, ; 6708 PB Wageningen, The Netherlands
                [3 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Laboratory of Bioinformatics, , Wageningen University and Research, ; 6708 PB Wageningen, The Netherlands
                [4 ]ISNI 0000 0001 0660 6765, GRID grid.419498.9, , Max Planck Institute for Plant Breeding Research, ; 50829 Köln, Germany
                Article
                1235
                10.1186/s13059-017-1235-x
                5452352
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                Funding
                Funded by: nwo
                Award ID: the NWO grant (849.13.005) for the project ERACAPS13.012, FLOWPLAST
                Categories
                Research
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                © The Author(s) 2017

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