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      Mind the gap: Epigenetic regulation of chromatin accessibility in plants

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          Abstract

          Chromatin plays a crucial role in genome compaction and is fundamental for regulating multiple nuclear processes. Nucleosomes, the basic building blocks of chromatin, are central in regulating these processes, determining chromatin accessibility by limiting access to DNA for various proteins and acting as important signaling hubs. The association of histones with DNA in nucleosomes and the folding of chromatin into higher-order structures are strongly influenced by a variety of epigenetic marks, including DNA methylation, histone variants, and histone post-translational modifications. Additionally, a wide array of chaperones and ATP-dependent remodelers regulate various aspects of nucleosome biology, including assembly, deposition, and positioning. This review provides an overview of recent advances in our mechanistic understanding of how nucleosomes and chromatin organization are regulated by epigenetic marks and remodelers in plants. Furthermore, we present current technologies for profiling chromatin accessibility and organization.

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          Most cited references195

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          Regulation of chromatin by histone modifications.

          Chromatin is not an inert structure, but rather an instructive DNA scaffold that can respond to external cues to regulate the many uses of DNA. A principle component of chromatin that plays a key role in this regulation is the modification of histones. There is an ever-growing list of these modifications and the complexity of their action is only just beginning to be understood. However, it is clear that histone modifications play fundamental roles in most biological processes that are involved in the manipulation and expression of DNA. Here, we describe the known histone modifications, define where they are found genomically and discuss some of their functional consequences, concentrating mostly on transcription where the majority of characterisation has taken place.
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            Crystal structure of the nucleosome core particle at 2.8 A resolution.

            The X-ray crystal structure of the nucleosome core particle of chromatin shows in atomic detail how the histone protein octamer is assembled and how 146 base pairs of DNA are organized into a superhelix around it. Both histone/histone and histone/DNA interactions depend on the histone fold domains and additional, well ordered structure elements extending from this motif. Histone amino-terminal tails pass over and between the gyres of the DNA superhelix to contact neighbouring particles. The lack of uniformity between multiple histone/DNA-binding sites causes the DNA to deviate from ideal superhelix geometry.
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              Chromatin accessibility and the regulatory epigenome

              Physical access to DNA is a highly dynamic property of chromatin that plays an essential role in establishing and maintaining cellular identity. The organization of accessible chromatin across the genome reflects a network of permissible physical interactions through which enhancers, promoters, insulators and chromatin-binding factors cooperatively regulate gene expression. This landscape of accessibility changes dynamically in response to both external stimuli and developmental cues, and emerging evidence suggests that homeostatic maintenance of accessibility is itself dynamically regulated through a competitive interplay between chromatin-binding factors and nucleosomes. In this Review, we examine how the accessible genome is measured and explore the role of transcription factors in initiating accessibility remodelling; our goal is to illustrate how chromatin accessibility defines regulatory elements within the genome and how these epigenetic features are dynamically established to control gene expression.
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                Author and article information

                Contributors
                Journal
                Plant Physiol
                Plant Physiol
                plphys
                Plant Physiology
                Oxford University Press (US )
                0032-0889
                1532-2548
                April 2024
                17 January 2024
                17 January 2024
                : 194
                : 4
                : 1998-2016
                Affiliations
                Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València , Valencia, 46022Spain
                Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València , Valencia, 46022Spain
                Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València , Valencia, 46022Spain
                Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València , Valencia, 46022Spain
                Author notes
                Author for correspondence: jagalbar@ 123456ibmcp.upv.es

                Joan Candela-Ferre and Borja Diego-Martin contributed equally to this work.

                Conflict of interest statement. None declared.

                Author information
                https://orcid.org/0009-0005-0917-8432
                https://orcid.org/0000-0002-8479-3604
                https://orcid.org/0009-0004-2298-5004
                https://orcid.org/0000-0003-2225-7168
                Article
                kiae024
                10.1093/plphys/kiae024
                10980423
                38236303
                83ca679c-6e73-4166-90d7-85417df0605d
                © The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence ( https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 09 October 2023
                : 23 November 2023
                : 22 February 2024
                Page count
                Pages: 19
                Funding
                Funded by: Spanish Ministry of Science and Innovation, DOI 10.13039/501100004837;
                Award ID: FPU19/05694
                Funded by: Spanish Ministry of Universities;
                Award ID: CIACIF/2021/432
                Funded by: Generalitat Valenciana, DOI 10.13039/501100003359;
                Categories
                Update
                AcademicSubjects/SCI01270
                AcademicSubjects/SCI01280
                AcademicSubjects/SCI02286
                AcademicSubjects/SCI02287
                AcademicSubjects/SCI02288
                Plphys/53

                Plant science & Botany
                Plant science & Botany

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