The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization

The endosperm is a seed tissue unique to flowering plants. Due to its central role in nourishing and protecting the embryo, endosperm development is subject to parental conflicts and adaptive processes, which led to the evolution of parent-of-origin-dependent gene regulation. The role of higher-order chromatin organization in regulating the endosperm genome was long ignored due to technical hindrance. We developed a combination of approaches to analyze nuclear structure and chromatin organization in Arabidopsis thaliana endosperm. Endosperm nuclei showed a less condensed chromatin than other types of nuclei and a peculiar heterochromatin organization, with smaller chromocenters and additional heterochromatic foci interspersed in euchromatin. This is accompanied by a redistribution of the heterochromatin mark H3K9me1 from chromocenters toward euchromatin and interspersed heterochromatin. Thus, endosperm nuclei have a specific nuclear architecture and organization, which we interpret as a relaxed chromocenter-loop model. The analysis of endosperm with altered parental genome dosage indicated that the additional heterochromatin may be predominantly of maternal origin, suggesting differential regulation of maternal and paternal genomes, possibly linked to genome dosage regulation.     

From nucleosome to chromosome: a dynamic organization of genetic information

Gene activity is controlled at different levels of chromatin organization, which involve genomic sequences, nucleosome structure, chromatin folding and chromosome arrangement. These levels are interconnected and influence each other. At the basic level nucleosomes generally occlude the DNA sequence from interacting with DNA-binding proteins. Evidently, nucleosome positioning is a major factor in gene control and chromatin organization. Understanding the biological rules that govern the deposition and removal of the nucleosomes to and from the chromatin fiber is the key to understanding gene regulation and chromatin organization. In this review we describe and discuss the relationship between the different levels of chromatin organization in plants and animals.     

The 4D Nucleome: Genome Compartmentalization in an Evolutionary Context

4D nucleome research aims to understand the impact of nuclear organization in space and time on nuclear functions, such as gene expression patterns, chromatin replication, and the maintenance of genome integrity. In this review we describe evidence that the origin of 4D genome compartmentalization can be traced back to the prokaryotic world. In cell nuclei of animals and plants chromosomes occupy distinct territories, built up from ~1 Mb chromatin domains, which in turn are composed of smaller chromatin subdomains and also form larger chromatin domain clusters. Microscopic evidence for this higher order chromatin landscape was strengthened by chromosome conformation capture studies, in particular Hi-C. This approach demonstrated ~1 Mb sized, topologically associating domains in mammalian cell nuclei separated by boundaries. Mutations, which destroy boundaries, can result in developmental disorders and cancer. Nucleosomes appeared first as tetramers in the Archaea kingdom and later evolved to octamers built up each from two H2A, two H2B, two H3, and two H4 proteins. Notably, nucleosomes were lost during the evolution of the Dinoflagellata phylum. Dinoflagellate chromosomes remain condensed during the entire cell cycle, but their chromosome architecture differs radically from the architecture of other eukaryotes. In summary, the conservation of fundamental features of higher order chromatin arrangements throughout the evolution of metazoan animals suggests the existence of conserved, but still unknown mechanism(s) controlling this architecture. Notwithstanding this conservation, a comparison of metazoans and protists also demonstrates species-specific structural and functional features of nuclear organization.     

Chromatin replication and epigenome maintenance

Stability and function of eukaryotic genomes are closely linked to chromatin structure and organization. During cell division the entire genome must be accurately replicated and the chromatin landscape reproduced on new DNA. Chromatin and nuclear structure influence where and when DNA replication initiates, whereas the replication process itself disrupts chromatin and challenges established patterns of genome regulation. Specialized replication-coupled mechanisms assemble new DNA into chromatin, but epigenome maintenance is a continuous process taking place throughout the cell cycle. If DNA synthesis is perturbed, cells can suffer loss of both genome and epigenome integrity with severe consequences for the organism.     

Epigenetic regulation of genes during development： A conserved theme from flies to mammals

Eukaryotic genome is organized in form of chromatin within the nucleus. This organization is important for compaction of DNA as well as for the proper expression of the genes. During early embryonic development, genomic packaging receives variety of signals to eventually set up cell type specific expression patterns of genes. This process of regulated chromatinization leads to "cell type specific epigenomes". The expression states attained during differentiation process need to be maintained subsequently throughout the life of the organism. Epigenetie modifications are responsible for chromatin dependent regulatory mechanism and play a key role in maintenance of the expression state-a process referred to as cellular memory. Another key feature in the packaging of the genome is formation of chro- matin domains that are thought to be structural as well as functional units of the higher order chromatin organization. Boundary elements that function to define such domains set the limits of regulatory elements and that of epigenetie modifications. This connection of epige- netic modification, chromatin structure and genome organization has emerged from several studies. Hox genes are among the best studied in this context and have led to the significant understanding of the epigenetic regulation during development. Here we discuss the evolu- tionarily conserved features of epigenetic mechanisms emerged from studies on homeotic gene clusters.     

Creating Order from Chaos: Epigenome Dynamics in Plants with Complex Genomes

Flowering plants have strikingly distinct genomes, although they contain a similar suite of expressed genes. The diversity of genome structures and organization is largely due to variation in transposable elements (TEs) and whole-genome duplication (WGD) events. We review evidence that chromatin modifications and epigenetic regulation are intimately associated with TEs and likely play a role in mediating the effects of WGDs. We hypothesize that the current structure of a genome is the result of various TE bursts and WGDs and it is likely that the silencing mechanisms and the chromatin structure of a genome have been shaped by these events. This suggests that the specific mechanisms targeting chromatin modifications and epigenomic patterns may vary among different species. Many crop species have likely evolved chromatin-based mechanisms to tolerate silenced TEs near actively expressed genes. These interactions of heterochromatin and euchromatin are likely to have important roles in modulating gene expression and variability within species.     

Predicting chromatin organization using histone marks

Genome-wide mapping of three dimensional chromatin organization is an important yet technically challenging task. To aid experimental effort and to understand the determinants of long-range chromatin interactions, we have developed a computational model integrating Hi-C and histone mark ChIP-seq data to predict two important features of chromatin organization: chromatin interaction hubs and topologically associated domain (TAD) boundaries. Our model accurately and robustly predicts these features across datasets and cell types. Cell-type specific histone mark information is required for prediction of chromatin interaction hubs but not for TAD boundaries. Our predictions provide a useful guide for the exploration of chromatin organization.

Electronic supplementary material

The online version of this article (doi:10.1186/s13059-015-0740-z) contains supplementary material, which is available to authorized users.     

Chromatin challenges during DNA replication and repair

Inheritance and maintenance of the DNA sequence and its organization into chromatin are central for eukaryotic life. To orchestrate DNA-replication and -repair processes in the context of chromatin is a challenge, both in terms of accessibility and maintenance of chromatin organization. To meet the challenge of maintenance, cells have evolved efficient nucleosome-assembly pathways and chromatin-maturation mechanisms that reproduce chromatin organization in the wake of DNA replication and repair. The aim of this Review is to describe how these pathways operate and to highlight how the epigenetic landscape may be stably maintained even in the face of dramatic changes in chromatin structure.     

Minimalistic 3D chromatin models: Sparse interactions in single cells drive the chromatin fold and form many-body units

Computational three-dimensional chromatin modeling has helped uncover principles of genome organization. Here, we discuss methods for modeling three-dimensional chromatin structures, with focus on a minimalistic polymer model which inverts population Hi-C into single-cell conformations. Utilizing only basic physical properties, this model reveals that a few specific Hi-C interactions can fold chromatin into conformations consistent with single-cell imaging, Dip-C, and FISH measurements. Aggregated single-cell chromatin conformations also reproduce Hi-C frequencies. This approach allows quantification of structural heterogeneity and discovery of many-body interaction units and has revealed additional insights, including (1) topologically associating domains as a byproduct of folding driven by specific interactions, (2) cell subpopulations with different structural scaffolds are developmental stage dependent, and (3) the functional landscape of many-body units within enhancer-rich regions. We also discuss these findings in relation to the genome structure–function relationship.