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BBA - Gene Regulatory Mechanisms (v.1809, #8)
Plant histone acetylation: In the beginning… by Jakob H. Waterborg (pp. 353-359).
The study of histone acetylation in plants started with protein purification and sequencing, with gel analysis and the use of radioactive tracers. In alfalfa, acid urea Triton gel electrophoresis and in vivo labeling with tritated acetate and lysine quantified dynamic acetylation of core histones and identified the replication-coupled and -independent expression patterns of the histone H3.1 and H3.2 variants. Pulse-chase analyses demonstrated protein turnover of newly synthesized histone H3.2 and thereby identified the replacement H3 histones of plants which maintain the nucleosome density of transcribed chromatin. Sequence analysis of histone H4 revealed acetylation of lysine 20, a site typically methylated in animals and yeasts. Histone deacetylase inihibitors butyrate and trichostatin A are metabolized in alfalfa, but loss of TSA is slow, allowing its use to induce transient hyperacetylation of histones H2B, H4 and H3. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants.► Personal historical perspective histone acetylation in plants. ► AUT gels and tritiated acetate define dynamic histone acetylation in plants. ► Identification of plant replacement histone H3 in plants. ► Butyrate and TSA in alfalfa induce histone hyper- and hypo-acetylation.
Keywords: Histone acetylation; Alfalfa; AUT gel; Replacement histone; H3
DNA methylation in higher plants: Past, present and future by Boris F. Vanyushin; Vasili V. Ashapkin (pp. 360-368).
A relatively high degree of nuclear DNA (nDNA) methylation is a specific feature of plant genomes. Targets for cytosine DNA methylation in plant genomes are CG, CHG and CHH (H is A, T, C) sequences. More than 30% total m5C in plant DNA is located in non-CG sites. DNA methylation in plants is species-, tissue-, organelle- and age-specific; it is involved in the control of all genetic functions including transcription, replication, DNA repair, gene transposition and cell differentiation. DNA methylation is engaged in gene silencing and parental imprinting, it controls expression of transgenes and foreign DNA in cell. Plants have much more complicated and sophisticated system of the multicomponent genome methylations compared to animals; DNA methylation in plant mitochondria is performed in other fashion as compared to that in nuclei. The nDNA methylation is carried out by cytosine DNA methyltransferases of, at least, three families. In contrast to animals the plants with the major maintenance methyltransferase MET1 (similar to animal Dnmt1) inactivated do survive. One and the same plant gene may be methylated at both adenine and cytosine residues; specific plant adenine DNA methyltransferase was described. Thus, two different systems of the genome modification based on methylation of cytosines and adenines seem to coexist in higher plants. This article is part of a Special Issue entitled: Epigenetic control of cellular and developmental processes in plants.► Replicative cytosine DNA methylation in plants. ► DNA demethylation by excision of m5C residues. ► Biological significance of DNA methylation. ► Genome-wide cytosine methylation patterns or DNA methylomes. ► Adenine DNA methylation in plants.
Keywords: DNA methylation; DNA methyltransferase; Epigenetics; Plant; 5-methylcytosine; N; 6; -methyladenine
Epigenetic control of gene regulation in plants by Massimiliano Lauria; Vincenzo Rossi (pp. 369-378).
In eukaryotes, including plants, the genome is compacted into chromatin, which forms a physical barrier for gene transcription. Therefore, mechanisms that alter chromatin structure play an essential role in gene regulation. When changes in the chromatin states are inherited trough mitotic or meiotic cell division, the mechanisms responsible for these changes are defined as epigenetic. In this paper, we review data arising from genome-wide analysis of the epigenetic landscapes in different plant species to establish the correlation between specific epigenetic marks and transcription. In the subsequent sections, mechanisms of epigenetic control of gene regulation mediated by DNA-binding transcription factors and by transposons located in proximity to genes are illustrated. Finally, plant peculiarities for epigenetic control of gene regulation and future perspectives in this research area are discussed. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants.► Mechanisms modulating chromatin structure control gene regulation. ► Distinct epigenetic modifications show specific correlations with transcription. ► Transcription factors and chromatin modifiers interact to control gene expression. ► Repeats regulate expression of adjacent genes through epigenetic marks diffusion. ► Specific epigenetic regulation may be associated with plant life cycle features.
Keywords: Epigenetics; Gene regulation; Chromatin; Transcription factor; Transposable element
A chromatin perspective of plant cell cycle progression by Celina Costas; Bénédicte Desvoyes; Crisanto Gutierrez (pp. 379-387).
The finely regulated series of events that span from the birth of a cell to the production of two new born cells encompass the cell cycle. Cell cycle progression occurs in a unidirectional manner and requires passing through a number of stages in response to cellular, developmental and environmental cues. In addition to these signaling cascades, transcriptional regulation plays a major role and acts coordinately with genome duplication during S-phase and chromosome segregation during mitosis. In this context, chromatin is revealing as a highly dynamic and major player in cell cycle regulation not only owing to the changes that occur as a consequence of cell cycle progression but also because some specific chromatin modifications are crucial to move across the cell cycle. These are particularly relevant for controlling transcriptional activation and repression as well as initiation of DNA replication and chromosome compaction. As a consequence the epigenetic landscape of a proliferating cell is very complex throughout the cell cycle. These aspects of chromatin dynamics together with the impact of epigenetic modifications on cell proliferation will be discussed in this article. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants.► Chromatin is revealing as highly dynamic during cell cycle progression. ► Specific chromatin modifications are crucial to move across the cell cycle. ► These refer to transcriptional control, genome duplication and chromsome compaction. ► The epigenetic landscape of a proliferating cell is very complex.
Keywords: Cell cycle; Chromatin; Epigenetics; Gene expression; DNA replication; Arabidopsis; Plant
Epigenetic control of Agrobacterium T-DNA integration by Shimpei Magori; Vitaly Citovsky (pp. 388-394).
To genetically transform plants, Agrobacterium transfers its T-DNA into the host cell and integrates it into the plant genome, resulting in neoplastic growths. Over the past 2 decades, a great deal has been learned about the molecular mechanism by which Agrobacterium produces T-DNA and transports it into the host nucleus. However, T-DNA integration, which is the limiting, hence, the most critical step of the transformation process, largely remains an enigma. Increasing evidence suggests that Agrobacterium utilizes the host DNA repair machinery to facilitate T-DNA integration. Meanwhile, it is well known that chromatin modifications, including the phosphorylation of histone H2AX, play an important role in DNA repair. Thus, by implication, such epigenetic codes in chromatin may also have a considerable impact on T-DNA integration, although the direct evidence to demonstrate this hypothesis is still lacking. In this review, we summarize the recent advances in our understanding of Agrobacterium T-DNA integration and discuss the potential link between this process and the epigenetic information in the host chromatin. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants. ► Agrobacterium utilizes the host DNA repair machinery to facilitate T-DNA integration. ► Chromatin modifications play an important role in DNA repair. ► We discuss the potential role of chromatin modifications in T-DNA integration.
Keywords: Agrobacterium; T-DNA integration; DSB repair; Chromatin modification; Histone code
Polycomb-group mediated epigenetic mechanisms through plant evolution by Yana Butenko; Nir Ohad (pp. 395-406).
PolycombGroup (PcG) proteins form an epigenetic “memory system”, conserved in both plants and animals, controlling global gene expression during development via histone modifications. The role of PcG proteins in plants was primarily explored in Arabidopsis thaliana, where PcG regulation of developmental processes was demonstrated throughout the plant life cycle. Our knowledge about the PcG machinery in terrestrial plants other than Arabidopsis began to accumulate only in recent years. In this review we summarize recent emerging data on the evolution and diversification of PcG mechanisms in various phyla, from early-diverging plants, including members of the Chlorophyte algae, through bryophytes and flowering plants. We describe the compositions of the PcG gene families, their so-far studied expression profiles, and finally summarize commonalities vs. differences among PcG functions across the various species. This article is part of a Special Issue entitled: Epigenetic control of cellular and developmental processes in plants.► The Polycomb Group complex (PcG) forms a “memory system” epigenetically via histone modifications. ► Here we review the evolution and diversification of the PcG mechanisms during plant evolution. ► We describe the compositions of PcG gene families, and compare their expression profiles. ► We summarize commonalities vs. differences among PcG functions across the various plant species.
Keywords: Abbreviations; AG; AGAMOUS; CLF; CURLY LEAF; EMF1; EMBRYONIC FLOWER1; EMF2; EMBRYONIC FLOWER2; ESC; EXTRA SEX COMB; E(z); ENHANCER OF ZESTE; FIE; FERTILIZATION INDEPENDENT ENDOSPERM; FIS2; FERTILIZATION INDEPENDENT SEED2; KNOX; KNOTTED-like; MEA; MEDEA; MSI1; MULTICOPY SUPPRESSOR OF IRA1; PcG; Polycomb group; PRC1; Polycomb Repressive Complex 1; PRC2; Polycomb Repressive Complex 2; SWN; SWINGER; Su(z)12; SUPRESSOR OF ZESTE 12; VRN2; VERNALIZATION2PcG; Evolution; Gene expression; Epigenetic; Plant development; H3K27 methylation
SET domain proteins in plant development by Tage Thorstensen; Paul E. Grini; Reidunn Birgitta Aalen (pp. 407-420).
Post-translational methylation of lysine residues on histone tails is an epigenetic modification crucial for regulation of chromatin structure and gene expression in eukaryotes. The majority of the histone lysine methyltransferases (HKMTases) conferring such modifications are proteins with a conserved SET domain responsible for the enzymatic activity. The SET domain proteins in the model plant Arabidopsis thaliana can be assigned to evolutionarily conserved classes with different specificities allowing for different outcomes on chromatin structure. Here we review the present knowledge of the biochemical and biological functions of plant SET domain proteins in developmental processes. This article is part of a Special Issue entitled: Epigenetic control of cellular and developmental processes in plants.► SU(VAR)3–9 proteins control transposons and epialleles importance for development. ► H3K27me1 HKMTases are controlling replication of heterochromatin DNA. ► ATXR3 and ASHH2 are of fundamental importance for growth and reproduction. ► SET domain proteins are positive and negative regulators of flowering time. ► E(z) proteins work in PRC2 complexes to control transitions in plant development.
Keywords: Histone methyltransferase; Epigenetics; Chromatin modulation; SET domain protein
Epigenetic gene regulation by plant Jumonji group of histone demethylase by Xiangsong Chen; Yongfeng Hu; Dao-Xiu Zhou (pp. 421-426).
Histone methylation plays an important role in epigenetic regulation of gene expression. Reversible methylation/demethylation of several histone lysine residues is mediated by distinct histone methyltransferases and histone demethylases. Jumonji proteins have been characterized to be involved in histone demethylation. Plant Jumonji homologues are found to have important functions in epigenetic processes, gene expression and plant development and to play an essential role in interplay between histone modifications and DNA methylation. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants.► JmjC protein function in plant gene expression and development. ► JmjC proteins in histone modification crosstalk. ► JmjC proteins in interaction between histone modification and DNA methylation.
Keywords: JmjC; Jumonji; Histone methylation; Demethylase; DNA methylation; Chromatin; Epigenetics; Arabidopsis; Rice
Epigenetics in plants—vernalisation and hybrid vigour by Michael Groszmann; Ian K. Greaves; Nicolas Albert; Ryo Fujimoto; Chris A. Helliwell; Elizabeth S. Dennis; W. James Peacock (pp. 427-437).
In this review we have analysed two major biological systems involving epigenetic control of gene activity. In the first system we demonstrate the interplay between genetic and epigenetic controls over the transcriptional activity of FLC, a major repressor of flowering in Arabidopsis. FLC is down-regulated by low temperature treatment (vernalisation) releasing the repressor effect on flowering. We discuss the mechanisms of the reduced transcription and the memory of the vernalisation treatment through vegetative development. We also discuss the resetting of the repressed activity level of the FLC gene, following vernalisation, to the default high activity level and show it occurs during both male and female gametogenesis but with different timing in each.In the second part of the review discussed the complex multigenic system which is responsible for the patterns of gene activity which bring about hybrid vigour in crosses between genetically similar but epigenetically distinct parents. The epigenetic systems that we have identified as contributing to the heterotic phenotype are the 24nt siRNAs and their effects on RNA dependent DNA methylation (RdDM) at the target loci leading to changed expression levels.We conclude that it is likely that epigenetic controls are involved in expression systems in many aspects of plant development and plant function.► Vernalisation induces epigenetic down regulation of FLC promoting flowering. ► Arabidopsis and wheat and barley have different epigenetic controls for flowering. ► 24nt siRNAs are reduced in Arabidopsis F1 hybrids showing heterosis. ► F1 hybrids have altered DNA methylation patterns in the neighbourhood of genes
Keywords: Arabidopsis; Heterosis; Flowering; Methylation; Paramutation; Epialleles
Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants by Kohler Claudia Köhler; David Kradolfer (pp. 438-443).
The sudden rise of angiosperms to ecological dominance was an “abominable mystery” to Charles Darwin, and understanding the underlying evolutionary driving force has remained a scientific challenge since then. The recognition of polyploidization as an important factor for plant speciation is likely to hold a key to this mystery and we will discuss possible mechanisms underlying this phenomenon. Polyploidization raises an immediate reproductive barrier in the endosperm, pointing towards an important but greatly underestimated role of the endosperm in preventing interploidy hybridizations. Parent-of-origin-specific gene expression is largely restricted to the endosperm, providing an explanation for the dosage sensitivity of the endosperm. Here, we review epigenetic mechanisms causing endosperm dosage sensitivity, their possible consequences for raising interploidy and interspecies hybridization barriers and their impact on flowering plant evolution. This article is part of a Special Issue entitled: Epigenetic Control.► Polyploidization is an important factor for plant speciation. ► Polyploidization raises an immediate reproductive barrier in the endosperm. ► We review epigenetic mechanisms causing endosperm dosage sensitivity. ► We discuss mechanisms underlying interploidy and interspecies hybridization barriers.
Keywords: Imprinting; Endosperm; Interploidy hybridization; Interspecies hybridization; Dosage sensitivity; Postzygotic hybridization barrier
siRNA-mediated chromatin maintenance and its function in Arabidopsis thaliana by Tatsuo Kanno; Yoshiki Habu (pp. 444-451).
Small interfering RNAs (siRNAs) are widespread in various eukaryotes and are involved in maintenance of chromatin modifications, especially those for inert states represented by covalent modifications of cytosine and/or histones. In contrast to mammalian genomes, in which cytosine methylation is restricted mostly to CG dinucleotide sequences, inert chromatin in plants carries cytosine methylation in all sequence contexts, and siRNAs play a major role in directing cytosine methylation through the process of RNA-directed DNA methylation. Recent advances in this field have revealed that siRNA-mediated maintenance of inert chromatin has diverse roles in development as well as in plant responses to the environment. Various proteinaceous factors required for siRNA-mediated chromatin modification have been identified in Arabidopsis thaliana, and much effort has been invested in understanding their function and interaction, resulting in the assignment of many of these factors to specific biochemical activities and engagement with specific steps such as transcription of intergenic RNAs, RNA processing, and cytosine methylation. However, the precise functions of a number of factors remain undesignated, and interactions of distinct pathways for siRNA-mediated chromatin modification are largely unknown. In this review, we summarize the roles of siRNA-mediated chromatin modification in various biological processes of A. thaliana, and present some speculation on the functions and interactions of silencing factors that, while not yet assigned to defined biochemical activities, have been loosely assigned to specific events in siRNA-mediated chromatin modification pathways. Special Issue entitled: Epigenetic control of cellular and developmental processes in plants.► Plant siRNA-mediated chromatin regulation affects various basic biological processes. ► Silent chromatin is maintained by combinatorial ways involving distinct silencing pathways. ► Structures of undesignated factors predict their functions in chromatin regulation.
Keywords: Abbreviations; ADK; ADENOSINE KINASE; AGO; ARGONAUTE; CMM2; conserved MOM1 motif2; CMT3; CHROMOMETHYLASE3; DCL3; DICER-LIKE3; Dcr; Dicer; DDM1; DECREASE IN DNA METHYLATION1; DDR; DRD1/DMS3/RDM1; DMS; DEFECTIVE IN MERISTEM SILENCING; DRD1; DEFECTIVE IN RNA-DIRECTED DNA METHYLATION1; DRM; DOMAINS REARRANGED DNA METHYLATION; H3K9me2; di-methylated histone H3 lysine 9; IBM1; INCREASE IN BONSAI METHYLATION1; IWR; Interacts With RNA polymerase II; KYP; KRYPTONITE; MET1; METHYLTRANSFERASE1; miRNA; microRNA; MMS; methyl methane sulfonate; MOM1; MORPHEUS' MOLECULE1; nat-siRNA; natural; cis; -antisense siRNA; piRNA; Piwi-interacting RNA; Pol II; RNA polymerase II; Pol IV; RNA polymerase IV; Pol V; RNA polymerase V; RdDM; RNA-directed DNA methylation; RDM; RNA-DIRECTED DNA METHYLATION; RDR2; RNA-dependent RNA polymerase2; RISC; RNA-induced silencing complex; ROS; REPRESSOR OF SILENCING; SDC; SUPPRESSOR OF drm1 drm2 cmt3; siRNA; small interfering RNA; SMC; structural maintenance of chromosome; SRA; SET and RING finger-associated; SWI2/SNF2; SWItch2/Sucrose NonFermentable2; TGS; transcriptional gene silencing; TSI; transcriptionally silent information Arabidopsis thaliana; Histone modification; Non-CG methylation; RNA-directed DNA methylation; siRNA
A “mille-feuille” of silencing: Epigenetic control of transposable elements by Mélanie Rigal; Olivier Mathieu (pp. 452-458).
Despite their abundance in the genome, transposable elements (TEs) and their derivatives are major targets of epigenetic silencing mechanisms, which restrain TE mobility at different stages of the life cycle. DNA methylation, post-translational modification of histone tails and small RNA-based pathways contribute to maintain TE silencing; however, some of these epigenetic marks are tightly interwoven and this complicates the delineation of the exact contribution of each in TE silencing. Recent studies have confirmed that host genomes have evolved versatility in the use of these mechanisms to individualize silencing of particular TEs. These studies also revealed that silencing of TEs is much more dynamic than had been previously thought and can be reversed on the genomic scale in particular cell types or under special environmental conditions. This article is part of a Special Issue entitled “Epigenetic control of cellular and developmental processes in plants”.► Transposable elements are major endogenous targets of epigenetic silencing mechanisms. ► Mechanisms maintaining certain epigenetic marks are tightly interwoven. ► Silencing of transposable elements is reversed in particular cells of the plant. ► Environmental changes can overcome transposable element silencing.
Keywords: Transposable elements; Silencing; Arabidopsis
Transgenerational epigenetic inheritance in plants by Marie-Theres Hauser; Werner Aufsatz; Claudia Jonak; Christian Luschnig (pp. 459-468).
Interest in transgenerational epigenetic inheritance has intensified with the boosting of knowledge on epigenetic mechanisms regulating gene expression during development and in response to internal and external signals such as biotic and abiotic stresses. Starting with an historical background of scantily documented anecdotes and their consequences, we recapitulate the information gathered during the last 60years on naturally occurring and induced epialleles and paramutations in plants. We present the major players of epigenetic regulation and their importance in controlling stress responses. The effect of diverse stressors on the epigenetic status and its transgenerational inheritance is summarized from a mechanistic viewpoint. The consequences of transgenerational epigenetic inheritance are presented, focusing on the knowledge about its stability, and in relation to genetically fixed mutations, recombination, and genomic rearrangement. We conclude with an outlook on the importance of transgenerational inheritance for adaptation to changing environments and for practical applications. This article is part of a Special Issue entitled “Epigenetic control of cellular and developmental processes in plants”.► The relevance of plant adaptation for coping with adverse environments ► Insights into mechanisms by which biotic and abiotic stress might impinge on the epigenome of plants ► The potential role of inherited epigenetic adjustments for plant adaptation
Keywords: Plant stress; Heritable stress effects; Epigenetics; Genome stability