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      Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato

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          Abstract

          Background

          Cold stress can greatly affect plant growth and development. Plants have developed special systems to respond to and tolerate cold stress. While plant scientists have discovered numerous genes involved in responses to cold stress, few studies have been dedicated to investigation of genome-wide chromatin dynamics induced by cold or other abiotic stresses.

          Results

          Genomic regions containing active cis-regulatory DNA elements can be identified as DNase I hypersensitive sites (DHSs). We develop high-resolution DHS maps in potato ( Solanum tuberosum) using chromatin isolated from tubers stored under room (22 °C) and cold (4 °C) conditions. We find that cold stress induces a large number of DHSs enriched in genic regions which are frequently associated with differential gene expression in response to temperature variation. Surprisingly, active genes show enhanced chromatin accessibility upon cold stress. A large number of active genes in cold-stored tubers are associated with the bivalent H3K4me3-H3K27me3 mark in gene body regions. Interestingly, upregulated genes associated with the bivalent mark are involved in stress response, whereas downregulated genes with the bivalent mark are involved in developmental processes. In addition, we observe that the bivalent mark-associated genes are more accessible than others upon cold stress.

          Conclusions

          Collectively, our results suggest that cold stress induces enhanced chromatin accessibility and bivalent histone modifications of active genes. We hypothesize that in cold-stored tubers, the bivalent H3K4me3-H3K27me3 mark represents a distinct chromatin environment with greater accessibility, which may facilitate the access of regulatory proteins required for gene upregulation or downregulation in response to cold stress.

          Electronic supplementary material

          The online version of this article (10.1186/s13059-019-1731-2) contains supplementary material, which is available to authorized users.

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          Most cited references49

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          High-resolution mapping and characterization of open chromatin across the genome.

          Mapping DNase I hypersensitive (HS) sites is an accurate method of identifying the location of genetic regulatory elements, including promoters, enhancers, silencers, insulators, and locus control regions. We employed high-throughput sequencing and whole-genome tiled array strategies to identify DNase I HS sites within human primary CD4+ T cells. Combining these two technologies, we have created a comprehensive and accurate genome-wide open chromatin map. Surprisingly, only 16%-21% of the identified 94,925 DNase I HS sites are found in promoters or first exons of known genes, but nearly half of the most open sites are in these regions. In conjunction with expression, motif, and chromatin immunoprecipitation data, we find evidence of cell-type-specific characteristics, including the ability to identify transcription start sites and locations of different chromatin marks utilized in these cells. In addition, and unexpectedly, our analyses have uncovered detailed features of nucleosome structure.
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            Identification of novel transcripts in annotated genomes using RNA-Seq.

            We describe a new 'reference annotation based transcript assembly' problem for RNA-Seq data that involves assembling novel transcripts in the context of an existing annotation. This problem arises in the analysis of expression in model organisms, where it is desirable to leverage existing annotations for discovering novel transcripts. We present an algorithm for reference annotation-based transcript assembly and show how it can be used to rapidly investigate novel transcripts revealed by RNA-Seq in comparison with a reference annotation. The methods described in this article are implemented in the Cufflinks suite of software for RNA-Seq, freely available from http://bio.math.berkeley.edu/cufflinks. The software is released under the BOOST license. cole@broadinstitute.org; lpachter@math.berkeley.edu Supplementary data are available at Bioinformatics online.
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              Charting histone modifications and the functional organization of mammalian genomes.

              A succession of technological advances over the past decade have enabled researchers to chart maps of histone modifications and related chromatin structures with increasing accuracy, comprehensiveness and throughput. The resulting data sets highlight the interplay between chromatin and genome function, dynamic variations in chromatin structure across cellular conditions, and emerging roles for large-scale domains and higher-ordered chromatin organization. Here we review a selection of recent studies that have probed histone modifications and successive layers of chromatin structure in mammalian genomes, the patterns that have been identified and future directions for research.
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                Author and article information

                Contributors
                jiangjm@msu.edu
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1474-7596
                1474-760X
                17 June 2019
                17 June 2019
                2019
                : 20
                : 123
                Affiliations
                [1 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Horticulture, , University of Wisconsin-Madison, ; Madison, WI 53706 USA
                [2 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Plant Biology, , Michigan State University, ; East Lansing, MI 48824 USA
                [3 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Horticulture, , Michigan State University, ; East Lansing, MI 48824 USA
                [4 ]ISNI 0000 0000 9479 9538, GRID grid.412600.1, Department of Biological Science, College of Life Sciences, , Sichuan Normal University, ; Chengdu, 610101 Sichuan China
                [5 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, State Key Laboratory for Crop Genetics and Germplasm Enhancement, , Nanjing Agriculture University, ; Nanjing, 210095 Jiangsu China
                [6 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Michigan State University AgBioResearch, ; East Lansing, MI 48824 USA
                Author information
                http://orcid.org/0000-0002-6435-6140
                Article
                1731
                10.1186/s13059-019-1731-2
                6580510
                31208436
                5712f403-f669-40bf-bf2d-043c45ac0161
                © The Author(s). 2019

                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.

                History
                : 28 February 2019
                : 5 June 2019
                Funding
                Funded by: FundRef //dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: ISO-1237969
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Genetics
                potato,cold stress,dnase i hypersensitive site,open chromatin,bivalent mark,h3k4me3,h3k27me3
                Genetics
                potato, cold stress, dnase i hypersensitive site, open chromatin, bivalent mark, h3k4me3, h3k27me3

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