Are Chromosomes In Plant And Animal Cells
Abstruse
Chromatin is the chief carrier of genetic information and is not-randomly distributed within the nucleus. Next-generation sequence-based chromatin conformation capture technologies accept enabled us to direct examine its 3-dimensional organization at an unprecedented scale and resolution. In the all-time-studied mammalian models, chromatin folding can exist broken down into three hierarchical levels, compartment, domains, and loops, which play important roles in transcriptional regulation. Although similar structures take now been identified in plants, they might not possess exactly the same functions equally the mammalian ones. Here, we review contempo Hello-C studies in plants, compare plant chromatin structures with their mammalian counterparts, and discuss the differences betwixt plants with different genome sizes.
Introduction
Chromosomes comprise different types of genetic information, such every bit genes, cis-regulatory elements, and repeats, all of which are stored in distinct locations inside the nucleus and require specific packaging and folding to office. For example, a regulatory element hundreds of kilobases away from a cistron would need to be folded back to the proximal promoter in gild to regulate the transcription of the cistron. It is now widely accepted that the spatial organization of chromatin plays important roles in biological processes such as DNA replication and repair, spatial- and temporal-specific factor expression, and in transposable chemical element (TE) repression. Hence, it is of great involvement to examine the three-dimensional (3D) arrangement of chromatin and associate its structural features to functions; this volition enable us to better understand the transcriptional regulation of central biological processes.
In the by two decades, the development of techniques that combine chromosome conformation capture (3C) and loftier-throughput sequencing has dramatically improved our understanding of chromosome spatial organization (Denker and De Laat, 2016). Among these techniques, Howdy-C is capable of capturing all chromatin interactions genome-wide at low resolution ( Lieberman-Aiden et al., 2009), while chromatin interaction analysis by paired-cease tag sequencing (ChIA-PET) ( Fullwood et al., 2009) and Howdy-C coupled to Bit-seq (HiChIP or PLAC-Seq) ( Fang et al., 2016; Mumbach et al., 2016) can generate loftier-resolution interaction maps in specific loci occupied past proteins that can be pulled down by Flake, such every bit modified histones, transcription factors, and RNA polymerase Ii. These techniques have generated extraordinary insights into the part of mammalian 3D chromatin system, but less is known about the roles of chromatin organization in plants.
In plants, early cytological studies accept shown that chromosomes at interphase are non-randomly organized; each chromosome occupies a singled-out and exclusive space within the nucleus, known as the chromosome territory ( Tiang et al., 2012). The plant genome varies remarkably in size and TE content due to whole-genome duplication, TE amplification, and DNA purging, and exhibits different chromosome territory patterns (Dong and Jiang, 1998; Fransz and Jong, 2011; Tiang et al., 2012). Chromosomes of big-genome plants, such equally barley and rye, showroom the "Rabl" configuration during interphase, in which the telomere and centromere rest at the opposite poles of the nuclei, reminiscent of the chromosome conformation at anaphase during mitosis (Dong and Jiang, 1998). By contrast, the small-genome plants often adopt various non-Rabl chromosome configurations. For example, in Arabidopsis, almost repeat elements are located in the pericentromeric region and class a densely packed singled-out chromocenter, while the euchromatin emanates outward, forming a "Rosette" configuration ( Fransz et al., 2002). Despite the low resolution and focus on centromere and telomere positions, these early studies clearly illustrated the diversity of 3D chromatin organization in plants.
Recently, 3C technologies accept been used to examine chromatin 3D organization in multiple crop species, in different tissues or in the same tissue under different growth conditions. In this review, we will discuss these new findings and compare institute 3C information side by side with the all-time-studied animal models at the levels of compartment, domain, and loops, in society to provide an overview of this emerging field.
Compartments
Mammalian A/B compartments
The showtime Hullo-C experiment showed that chromatin is non-randomly arranged within the mammalian nucleus, and the active and repressive regions are spatially segregated ( Lieberman-Aiden et al., 2009). A primal finding of this pilot study was that the agile chromatin prefers to interact with the other agile regions, and the repressive chromatin also interacts with itself. Thus the genome is partitioned into two different territories in space and exhibits a plaid pattern on the Hi-C interaction frequency matrix. The active and repressive territories are referred to as the A compartment and the B compartment, respectively.
The mammalian A compartment is actively transcribed and is enriched for open chromatin, agile histone modifications such as H3K4me3 and H3K27ac, and loftier GC content. The B compartment is associated with the nuclear lamina, is enriched for repressive histone marks such as H3K9me3, and is AT rich ( Lieberman-Aiden et al., 2009; Ryba et al., 2010). The A/B compartments tin exist further divided into sub-compartments at higher resolution, which likewise have unique histone modification patterns ( Rao et al., 2014). The Hi-C based compartment definition is consequent with previous microscopic and nuclear lamina association studies, which plant that active chromatin residues in the center of the nucleus and the heterochromatin is pushed toward the nuclear periphery (Bickmore and van Steensel, 2013). I could argue that the A/B compartments could be an artifact resulting from averaging the interaction signal from millions of cells analyzed in Hello-C. However, super-resolution imaging has confirmed that compartments can exist at the single-cell level and are polarized along the chromosome ( Wang et al., 2016).
Compartment partitioning is not static, and can switch frequently betwixt dissimilar tissues or developmental stages. For example, 36% of the human genome switched compartments in at least one of the lineages analyzed; loci that switched from A to B often showed decreased gene expression, while those that switched from B to A often showed increased expression ( Dixon et al., 2015). Intra-chromosome chromatin co-accessibility too positively correlates with the compartment dynamics, further suggesting that compartment organization could be linked to transcription ( Gate et al., 2018).
Global and local A/B compartments in plants
Using Hello-C, compartment-like structures have been identified in plant species with genomes of different sizes, such every bit Arabidopsis (135 Mb), rice (430 Mb), and maize (2.iv Gb) ( Feng et al., 2014; Grob et al., 2014; Dong et al., 2017; Liu et al., 2017). In institute chromosomes, the two actively transcribed euchromatin artillery oft form the A compartment and the pericentromeric heterochromatin forms the B compartment (Fig. 1) ( Feng et al., 2014; Grob et al., 2014). This partition is largely stable across tissues ( Dong et al., 2020), and reduced compartment interaction has been found in Arabidopsis Dna methylation mutants ( Feng et al., 2014) and in rice and maize endosperm tissues in which Deoxyribonucleic acid demethylation occurred naturally( Dong et al., 2020). These findings support the hypothesis that the genome-broad compartment partitioning could be due to spatial separation of the loose euchromatin and the condensed heterochromatin.
Fig. ane.
Global and local compartments in small- and big-genome plants. (A) The Arabidopsis chromosome tin can be partitioned into the A compartment, which consists of ii factor-rich euchromatin arms, and the B compartment, which contains the TE-rich heterochromatin and chromocenter. The A compartment tin can be further subdivided into the actively transcribed loose structural domains (LSDs) and the less active nuclear periphery-localized compact structural domains (CSDs). (B) In large-genome plants, the euchromatin arms and the pericentromeric heterochromatin can also form A/B compartments. Local A/B compartments tin also be identified in both the euchromatin and heterochromatin. Every bit an instance, the figure shows a region inside the global B compartment that is partitioned into local A/B compartments using the local Hi-C interaction matrix; the local B compartments are non associated with the nuclear periphery.
Fig. 1.
Global and local compartments in small-scale- and large-genome plants. (A) The Arabidopsis chromosome can exist partitioned into the A compartment, which consists of two gene-rich euchromatin arms, and the B compartment, which contains the TE-rich heterochromatin and chromocenter. The A compartment tin can be further subdivided into the actively transcribed loose structural domains (LSDs) and the less active nuclear periphery-localized compact structural domains (CSDs). (B) In big-genome plants, the euchromatin arms and the pericentromeric heterochromatin can also course A/B compartments. Local A/B compartments can also be identified in both the euchromatin and heterochromatin. Equally an example, the figure shows a region within the global B compartment that is partitioned into local A/B compartments using the local Hi-C interaction matrix; the local B compartments are non associated with the nuclear periphery.
Besides the A/B compartments, some other compartment-similar structure tin can be identified within the Arabidopsis A compartment (Fig. 1A). Based on the local Hi-C interaction matrix of individual Arabidopsis chromosome arms, regions disposed to acquaintance with the chromocenter were called compacted structural domains (CSDs), while the remaining regions, which are associated with active gene expression, were referred to as loose structural domains (LSDs) ( Grob et al., 2014). It has been shown that the CSDs are associated with the nuclear periphery, which requires lamina-similar proteins CRWN1 and CRWN4, as well every bit CHG and CHH DNA methylation ( Bi et al., 2017; Grob and Grossniklaus, 2019; Hu et al., 2019).
In plants with medium-sized and big genomes, such as tomato and maize, compartment partitioning can be fifty-fifty more complicated, as their euchromatin and heterochromatin are much larger and less homogeneous than those of Arabidopsis. For example, in tomato chromosomes, near of the heterochromatin is categorized as the B compartment using the genome-broad Hullo-C interaction matrix at low resolution (bin size 0.5 Mb). When a higher resolution or the local Hi-C interaction matrix is used, gene islands within the heterochromatin and TE/repeat regions in the euchromatin are identified equally local A and B compartments, respectively (Fig. 1B). This miracle is most pronounced in plants with large TE-rich genomes, such as maize, tomato, and sorghum (Dong et al., 2017, 2020).
Phase separation, nuclear lamina, and compartment formation
Several layers of force accept been proposed that contribute to the observed sectionalisation into A/B compartments. The B compartment was observed to overlap well with nuclear lamina-associated domains, suggesting that the A/B compartments might be formed by separating the chromatin into 2 parts, in the nuclear periphery and the nuclear interior (van Steensel and Belmont, 2017). Yet, in the inverted nuclei of mouse rod photoreceptor cells, the heterochromatin is located at the nuclear center and the euchromatin is located around the nuclear periphery. The A/B compartment note of these nuclei remained unchanged, suggesting that localization at the periphery or the interior of the nucleus might not drive A/B compartmentation ( Falk et al., 2019). Another hypothesis is that transcription activity drives germination of the A compartment, as the actively transcribed regions are located in the nuclear interior. It has been shown that knockdown of RNA PolII resulted in euchromatin being pushed toward the nuclear periphery ( Krüger et al., 2015; Stevens et al., 2017).
More than recently, it has been suggested that the attraction between heterochromatin is the primal driving force for mammalian chromatin compartmentalization ( Falk et al., 2019). This chromatin analogousness theory is in line with the liquid–liquid phase separation model, in which the concentration of macromolecules, also as other characteristics such as common salt blazon, co-solutes, and pH, helps macromolecules to condense into dense phases, which exist alongside neighboring dilute phases ( Alberti et al., 2019). In improver, chromatin bridges between H3K9me2/three nucleosomes can promote the formation of complanate chromatin globules that are separated from the surrounding chromatin, which means the loci within the globule adopt to contact each other and conduct like ane compartment ( Hiragami-Hamada et al., 2016).
In plants with large genomes, both global and local compartment partitions correlate well with heterochromatin/euchromatin condition, and these compartments exhibit features like those typical of mammalian compartments( Dong et al., 2017), suggesting that the chromatin attraction and phase separation model might explain their formation (Fig. 1B). However, the Arabidopsis LSD/CSD-type compartments, which lack a articulate distinction in euchromatin and heterochromatin status, might event from nuclear periphery positioning (Wang and Liu, 2019). In improver, electron microscopy confirmed that plant heterochromatin is not always pushed toward the nuclear periphery in the big-genome plants such as maize (Fig. ii), a finding that is consistent with the early cytology studies (Fransz and Jong, 2011). In improver, unlike the local compartments in the large-genome plants, the LSD/CSD compartments in Arabidopsis do non overlap with chromatin domains, which are another layer of 3D chromatin organization that volition be discussed in the post-obit sections.
Fig. 2.
Manual electron microscopy images of nuclei of maize and tomato plant. (A) Maize leaf mesophyll cell nucleus. Dark-stained regions, representing heterochromatin, are located inside the nucleus rather than at its periphery. (B) Tomato leafage mesophyll cell nucleus. Heterochromatin is positioned near the nuclear membrane. Note the differential distribution of night patches in the two nuclei, indicated by the arrowheads. The asterisk indicates the nucleolus. Calibration bar=i μm.
Fig. 2.
Transmission electron microscopy images of nuclei of maize and tomato. (A) Maize leaf mesophyll cell nucleus. Dark-stained regions, representing heterochromatin, are located inside the nucleus rather than at its periphery. (B) Tomato leafage mesophyll cell nucleus. Heterochromatin is positioned nigh the nuclear membrane. Note the differential distribution of dark patches in the 2 nuclei, indicated by the arrowheads. The asterisk indicates the nucleolus. Scale bar=one μm.
Domains
Mammalian TADs and the loop extrusion model
Chromatin domains are the about prominent feature in the mammalian genome, and are often referred to as topologically associated domains (TADs). The interaction frequency of loci inside a TAD is college than that of loci betwixt TADs and decays sharply at the domain boundaries ( Dixon et al., 2012; Nora et al., 2012). This interaction design hints at a potential function of TADs, which is to confine chromatin interactions, such as those between distal enhancers and proximal promoters, within a single domain.
This hypothesis is further supported by observations that the expression of genes within a TAD are weakly coordinated ( Dixon et al., 2012; Nora et al., 2012; Zhan et al., 2017) and the majority of promoter–enhancer interactions are restricted within TADs ( Ji et al., 2016). By inserting reporter genes into TADs, it was constitute that the sensor expression profile correlates well with the TAD environs, suggesting that TADs sectionalization the genome into isolating blocks inside which the regulatory elements are bars ( Symmons et al., 2014). It is worth noting that after the destruction of most TADs, the overall gene expression design is not changed ( Nora et al., 2017; Rao et al., 2017; Ghavi-Captain et al., 2019), indicating that TADs are non the only mechanism for regulating factor expression. It has also been shown that loci within a TAD exhibit similar histone modification patterns ( Le Dily et al., 2014; Rao et al., 2014) and that the boundaries of TADs overlap with the boundaries of DNA replication domains ( Pope et al., 2014).
The borders of some TADs were found to have CCCTC-bounden factor (CTCF) and cohesin binding, which could form a chromatin loop, and this type of domain is often called the "loop domain" (Fig. 3A) ( Rao et al., 2014). CTCF is an 11-zinc-finger (ZF) transcription factor that has an orientation-specific binding motif and is famous for its part in insulator function ( Heger et al., 2012). This finding subsequently led to the loop extrusion model of TAD formation ( Murayama et al., 2018; Davidson et al., 2019). The structural maintenance of chromosomes (SMC) subunits of the cohesin complex can course dimers through their hinge domain at i end, and interact with Deoxyribonucleic acid at the other stop ( Forest et al., 2010). When the cohesin complex binds to two unlike chromatin loci, the two subunits progressively slide forth the chromatin fiber to form a loop, which is eventually stalled by the directional CTCF binding ( Fudenberg et al., 2016). During this process, the interaction betwixt loci within two convergent CTCF binding sites is facilitated by the extrusion of the loop ( Fudenberg et al., 2016).
Fig. 3.
Compartment domains. (A) Loop domain in the mammalian genome. These domains are located within ane compartment, and CTCT loops are often formed at the domain corner. The small adjacent loop domains can grade larger domains and take a nested construction. The dynamics of a loop domain are associated with changes in CTCF binding. (B) Compartment domains in large-genome plants. These domains often overlap with local compartments, with agile genes located within domains that are associated with A compartments, while TEs and repressed genes are located in domains that overlap with B compartments. Compartment and domain changes oft correlate with changes in gene expression. (C) In Arabidopsis, the chromosome arms are partitioned into loose structural domain (LSDs) and compacted structural domain (CSDs) that are like to the local A/B compartments rather than the mammalian TAD and the compartment domains found in large-genome plants.
Fig. three.
Compartment domains. (A) Loop domain in the mammalian genome. These domains are located within one compartment, and CTCT loops are ofttimes formed at the domain corner. The pocket-sized adjacent loop domains can form larger domains and accept a nested structure. The dynamics of a loop domain are associated with changes in CTCF binding. (B) Compartment domains in big-genome plants. These domains oft overlap with local compartments, with active genes located within domains that are associated with A compartments, while TEs and repressed genes are located in domains that overlap with B compartments. Compartment and domain changes oftentimes correlate with changes in gene expression. (C) In Arabidopsis, the chromosome arms are partitioned into loose structural domain (LSDs) and compacted structural domain (CSDs) that are similar to the local A/B compartments rather than the mammalian TAD and the compartment domains found in large-genome plants.
A growing torso of show supports the loop extrusion model. Information technology has been institute that cohesin bounden is highly mobile in the human genome, and its binding sites frequently occur at the inner side of CTCF at the TAD edge ( Tang et al., 2015). Deposition of either CTCF or a cohesin subunit can disrupt the TAD structure ( Nora et al., 2017; Rao et al., 2017). Flipping the CTCF binding site tin also disrupt the TAD ( Guo et al., 2015). Contempo single molecular imaging studies too back up that cohesin extrusion contributes to loop formation ( Davidson et al., 2019; Kim et al., 2019).
It is important to keep in listen that all 3D structures, such every bit A/B compartments and domains identified by 3C experiments, are probable to correspond the average interaction pattern of a large number of cells. For case, with high-resolution Hi-C data, human being TADs can be farther partitioned into subdomains (sub-TADs or contact domains). These domains showroom a like self-association construction with a median size of ~200 kb, smaller than the TADs, which are at the megabase scale (Fig. 3A) ( Phillips-Cremins et al., 2013; Rao et al., 2014). In the smaller genome of Drosophila (180 Mb), the TAD-similar domains are similar in size to the man sub-TADs at l–100 kb, depending on the Hello-C resolution (Bonev and Cavalli, 2016). Recent single-cell Hi-C studies have now confirmed that TADs showroom substantial variation among prison cell populations ( Stevens et al., 2017; Tan et al., 2018). In addition, domain edge loci exercise not always co-localize, and TADs tin can intermission or merge into bulk TADs (Fig. 3A).
TAD-like chromatin domains in plants
TAD organization is non a prominent characteristic in Arabidopsis ( Feng et al., 2014; Grob et al., 2014). Using kilobase-resolution Hi-C, few domain-similar structures could be identified in Arabidopsis. Their boundaries are enriched for active genes and associated with active epigenetic marks such as open chromatin, H3K4me3, and H3K9ac, while the interior regions are not actively transcribed ( Wang et al., 2015). Compared with the mammalian TADs, the Arabidopsis domains are smaller and the interaction strength is weaker (Fig. 3C). In addition, a few TAD-like structures have besides been found in the Arabidopsis H3K27me3-rich and H3K9me2-rich chromocenter heterochromatic regions ( Feng et al., 2014; Rowley et al., 2017).
In large-genome plants such as maize and tomato, a lot more TAD-like structures tin be identified, and TAD-like domains could cover fifty–90% of their genomes depending on the calling algorithm and cutoff (Fig. 3B). Their domain boundaries are enriched for active genes and active histone marks, and are stable in dissimilar tissues, developmental stages, and growth conditions (Dong et al., 2017, 2018, 2020; Liu et al., 2017; Wang et al., 2018). Unlike the mammalian TADs, well-nigh of these plant domain-like structures overlap with the local A/B compartment, and should be referred to equally "compartment domains" (Fig. 3A) ( Dong et al., 2017).
Unique features of the plant compartment domains
Mammalian TADs and plant compartment domains are 2 different structures that should non be confused (Fig. 3). By definition, TADs and domains are structures marked by the stiff interaction within themselves and as well strong insulation at the border region, while compartment status is defined past a region's global interaction blueprint. Cohesin and CTCF are required for the germination of the mammalian loop domains. In studies, when cohesin or CTCF was depleted, compartment switches were often observed between neighboring loci, and small compartment domains associated with uniform epigenetic marks were formed, which were similar to the compartment domains found in plants ( Nora et al., 2017; Rao et al., 2017). CTCF is present simply in bilateria and is absent from plant genomes ( Heger et al., 2012; Heger and Wiehe, 2014). Although proteins such as AS1 and AS2 have been suggested to have a potential insulator function in the plant genome, the limited binding sites brand them unlikely to serve equally a general insulator protein ( Guo et al., 2008; Iwasaki et al., 2013). Besides, one study in rice showed that the enriched motifs at domain borders belong to the TCP transcription factor and bZIP proteins rather than those of the Zn finger proteins like CTCF ( Liu et al., 2017).
A unique characteristic of the plant compartment domain is that domains of the same type interact with each other at both intra- and inter-chromosome levels, forming a checkerboard design like that of the A/B compartments ( Dong et al., 2017). Mammalian TADs show no such pattern, and they often exhibit a nested structure (Fig. 3), while their loops usually occur at the inner side of the loop domain and are called "corner loops". In both maize and tomato, large chromatin loops betwixt factor islands can exist detected by Hi-C. All the same, these loops are enriched outside of the domain ( Dong et al., 2017), which is similar to the small-scale compartment domains of Drosophila ( Rowley et al., 2017).
Mammalian loop domains are conserved between different species, while the conservation of loop domains is associated with conservation of CTCF bounden sites. Institute compartment domains likewise take dissimilar chromatin states, similar to the ones in Drosophila, while their border regions are not conserved in related establish species ( Dong et al., 2017; Rowley et al., 2017). Neighboring plant compartment domains frequently possess dissimilar transcription activities, different the TAD boundaries in human being that are able to separate consecutive active or consecutive heterochromatin regions. It is most likely that without a CTCF-similar factor to physically clamp two chromatin fibers together, the interaction of plant domains would be weaker than that of the mammalian ones. When comparison Hi-C information of different institute tissues, it was found that the changes of domain edge are often associated with differential gene expression ( Dong et al., 2020). In addition, the Arabidopsis heterochromatin domains are diminished in methylation mutants, and the domain insulation becomes much weaker in endosperm tissues ( Feng et al., 2014; Dong et al., 2020). Together, these findings propose that transcriptional activeness and heterochromatin condition could be the main factors determining domain formation in plants.
Loops
Early studies of promoter chromatin loops
It is well known that distal regulatory elements tin can make physical contact with genes through chromatin looping. The all-time-studied example is the β-globin genes, which revealed a causal human relationship between looping and factor activation (Smallwood and Ren, 2013). With 3C coupled to sequencing, many chromatin loops take now been identified in the mammalian genome. As well equally promoter–enhancer interactions, promoter–promoter and enhancer–enhancer interactions are also prevalent, and the interacting gene pairs tend to be expressed in a coordinated manner ( Li et al., 2012; Ji et al., 2016). These transcription-related loops are often associated with a mediator complex and are cell type specific. The most prominent loops are those formed betwixt loci bound past the CTCF and cohesin. These loops exhibit the most intense interaction frequency and are relatively conserved between cell types ( Dowen et al., 2014). There are also some loops associated with repressive signals, such as polycomb repressive circuitous 2 (PRC2) marking H3K27me3 ( Entrevan et al., 2016). The outset identified long-range interaction in plant species is that formed between the maize b1 gene and upstream regulatory elements spanning ~100 kb. Agile expression of the b1 factor requires a proper loop structure, which is mediated in a tissue- and epiallele-specific manner ( Louwers et al., 2009).
Loops betwixt constitute heterochromatin regions
Long-range promoter–enhancer loops are not common in the model plant Arabidopsis ( Feng et al., 2014; Grob et al., 2014). The most prominent long-range interaction in the Arabidopsis genome is formed betwixt 10 heterochromatin islands from different chromosomes and is termed Interactive Heterochromatic Islands (IHI or KNOT) ( Feng et al., 2014; Grob et al., 2014). These loci are located in both euchromatic arms and pericentromeric heterochromatic chromocenters, and interact with each other as well as with the telomeric regions, whereas they do non interact with other pericentromeric regions ( Feng et al., 2014). They also course a separate compartment to the residual of the genome. Like loops have been observed in the monocot rice genome, where the IHI is also enriched for TE, sRNAs, and the repressive histone marking H3K9me2 ( Dong et al., 2018).
A recent study showed that IHI is able to silence transgenes through establishing concrete interactions with transgene loci, suggesting a potential function in defense against invasive Dna (Grob and Grossniklaus, 2019). Counterintuitively, heterochromatin condensation might not be required for IHI loops, since they remained intact in suvh4/suvh5/suvh6 triple mutants (which show reduced non-CG methylation and H3K9me2) as well as ddm1 and met1 mutants (which show reduced Deoxyribonucleic acid methylation in all sequence contents); in fact, more IHI loops were found in these mutants ( Feng et al., 2014).
It is worth noting that large-genome plants as well take similar heterochromatin notches in the euchromatic artillery without forming IHI-like structures. A recent H3K9me2 ChIA-PET experiment in maize identified over 10 000 H3K9me2-associated loops. Unlike the IHIs, most of them are formed between loci inside chromocenters ( Zhao et al., 2019). All the same, changes in these heterochromatin loops are not associated with factor expression changes, dissimilar the mammalian ones.
A variety of loops in constitute euchromatin
Despite the lack of long-range interaction, short-range loops have been found in Arabidopsis ( Crevillén et al., 2013; Ariel et al., 2014; Cao et al., 2014; Liu et al., 2014, 2016; Wang et al., 2019). The actively transcribed FLC locus forms a loop betwixt the 5′ and three′ stop of the factor. Upon common cold treatment, FLC is repressed by the polycomb poly peptide complex and the loop is disrupted ( Crevillén et al., 2013). Ultra-high-resolution Hi-C at sub-kilobase resolution has as well identified over twenty 000 chromatin loops ranging from 2 kb to 25 kb in Arabidopsis ( Liu et al., 2016). Such cistron self-looping frequently correlates with gene expression, suggesting either a potential regulatory office or that it is the active transcription that causes the head-to-tail cistron looping.
In large-genome plants, many long-range chromatin interactions are plant betwixt gene islands and can be identified as "loops" from the Hi-C interaction matrix (Dong et al., 2017, 2020; Wang et al., 2017). For example, in the lycopersicon esculentum genome, the highly expressed genes located in the heterochromatin neighborhood tend to interact with each other, while this blueprint is diminished in the factor-rich euchromatin (Fig. four). Their loop anchor loci are enriched for active histone modifications (H3K4me3 and H3K27ac), while tissue-specific loop changes are oftentimes associated with changes in factor expression (Dong et al., 2017, 2020; Wang et al., 2017). One interesting ascertainment is that if two gene loci are joined by a chromatin loop in maize, their syntenic gene pairs in related species (rice, sorghum, and millet) have a shorter genomic distance compared with those of the non-loop genes ( Dong et al., 2020). This suggests that the loop genes are under choice and that they could exist co-regulated. It should be noted that despite the large variation in genome size, most plants have like numbers of genes and open chromatin regions. As a outcome, genes and their distal regulatory elements are probable to exist separated past more TEs and repeats as the genome size increases.
Fig. iv.
Chromatin loops form between active factor islands in regions of depression factor density. Tomato plant genes are ranked according to their expression level in leaf tissue and neighborhood cistron density (one Mb upstream and downstream), and are equally divided into 4×4 groups based on the dual-index ranking ( Dong et al., 2017). The heatmap represents the average Hi-C interaction matrix for each group of genes centered on their gene transcriptional start sites (TSS). Highly expressed genes located in low-factor-density regions are more probable to be associated with chromatin loops. In other words, these Hi-C loops are often identified between two actively transcribed regions separated by TE-rich heterochromatin, consistent with the observation that these loops are often minor local compartments.
Fig. four.
Chromatin loops form between active gene islands in regions of low gene density. Lycopersicon esculentum genes are ranked according to their expression level in leaf tissue and neighborhood gene density (1 Mb upstream and downstream), and are every bit divided into four×iv groups based on the dual-index ranking ( Dong et al., 2017). The heatmap represents the boilerplate Hi-C interaction matrix for each group of genes centered on their gene transcriptional start sites (TSS). Highly expressed genes located in depression-gene-density regions are more likely to be associated with chromatin loops. In other words, these Hi-C loops are often identified betwixt two actively transcribed regions separated past TE-rich heterochromatin, consistent with the observation that these loops are frequently small local compartments.
However, it is challenging for Hi-C to resolve loops at the ten kb range, in big and repetitive genomes, where about of the constitute cis-regulatory elements reside. Recently, ChIA-PET and HiChIP, which have higher resolution than Hello-C, take been used to report the chromatin loops ( Li et al., 2019; Peng et al., 2019; Ricci et al., 2019; Zhao et al., 2019). A plethora of cistron-to-gene and cistron-to-distal open chromatin loops accept been identified in rice and maize by ChIA-PET. These chromatin loop loci are oftentimes enriched for expression quantitative trait loci, and the loop genes showroom a correlated expression design. Unlike the loops in beast species, the ten kb range loops detected by ChIA-PET are not enriched within plant domains, supporting the argument that, in dissimilarity to the mammalian TADs, the institute compartment domains are not used to confine enhancer–promoter interactions.
Concluding remarks
Plant interphase chromatin is non-randomly organized within the nucleus and occupies a distinct infinite ( Tiang et al., 2012). In the by two decades, the development of 3C-based techniques has enabled us to straight examine the 3D organisation of chromatin (Yu and Ren, 2017). Most of these techniques are based on the principle that spatially shut DNA fragments are ligated more efficiently than distal ones. Therefore, the relative spatial altitude between any two DNA loci could exist inferred from their ligatability. However, we should go along in mind that all these and so-called establish chromatin "3D structures" inferred from 3C information are based on the average ligatability of DNA in millions of cells, and often from a non-compatible cell population. Without single-cell-based assays, it is impossible to be certain whether these structures actually exist in individual cells.
Multiple Hi-C studies have now confirmed that found cells take like compartment, domain, and loop structures to those in mammalian cells ( Feng et al., 2014; Grob et al., 2014; Liu et al., 2016, 2017; Dong et al., 2017, 2018; Wang et al., 2017; Li et al., 2019). Many of the observed differences between found and fauna species could exist due to the lack of a CTCF-like insulator poly peptide in plants. As nosotros take passed the early discovery phase, the side by side big question is whether these structures have biological functions, rather than being the outcome of the spatial separation of euchromatin and heterochromatin.
The other equally important just often disregarded question is why plants have not evolved a CTCF equivalent and lack the mammalian TAD-like loop domains. As TADs and chromatin loops are vital for mammalian transcriptional regulation, would the lack of this important tool fundamentally alter the way gene expression is regulated in plants? After all, plants and animals have like numbers of protein-coding genes and of open chromatin regions per cell/tissue type. Nevertheless, open chromatin regions of plants show significantly less tissue-specific dynamics compared with the mammalian ones ( Mascher et al., 2017; Corces et al., 2018; Lü et al., 2018; Li et al., 2019; Peng et al., 2019; Yoshida et al., 2019). One possibility is that without TADs and CTCF loops it would be hard for a plant gene to "loop" with a different open chromatin region when its expression level needs to change in dissimilar tissues. Alternatively, the lack of tissue-specific open chromatin dynamics could be the reason why plants did not evolve TADs or CTCF. Hence, alternative mechanisms such as tissue-specific epigenetic marks would be used to regulate gene expression in plants. Perhaps that is the penalty for not evolving TADs and CTCF loops.
The quest to understand institute 3D chromatin organization and its functions is by no means complete. The importance of crop models and the long departure fourth dimension of plants and animals, and even inside establish kingdoms, ensure that there will be enough of novel discoveries in the years to come.
Acknowledgements
This work was supported past funding from South China Botanical Garden CAS, Hong Kong, General Enquiry Fund (GRF1404119), Surface area of Excellence Scheme (AoE/M-403/16) and the State Primal Laboratory of Agrobiotechnology.
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