Histone variants in plant transcriptional regulation

BBAGRM-01053; No. of pages: 8; 4C: 2, 4 Biochimica et Biophysica Acta xxx (2016) xxx–xxx

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Review

Histone variants in plant transcriptional regulation☆ Danhua Jiang, Frédéric Berger ⁎ Gregor Mendel Institute, Vienna Biocenter, Dr. Bohr-Gasse 3, 1030 Vienna, Austria

a r t i c l e

i n f o

Article history: Received 21 March 2016 Received in revised form 18 June 2016 Accepted 3 July 2016 Available online xxxx Keywords: Histone variants Histone chaperone Epigenetics Chromatin Transcription

a b s t r a c t Chromatin based organization of eukaryotic genome plays a profound role in regulating gene transcription. Nucleosomes form the basic subunits of chromatin by packaging DNA with histone proteins, impeding the access of DNA to transcription factors and RNA polymerases. Exchange of histone variants in nucleosomes alters the properties of nucleosomes and thus modulates DNA exposure during transcriptional regulation. Growing evidence indicates the important function of histone variants in programming transcription during developmental transitions and stress response. Here we review how histone variants and their deposition machineries regulate the nucleosome stability and dynamics, and discuss the link between histone variants and transcriptional regulation in plants. This article is part of a Special Issue entitled: Plant Gene Regulatory Mechanisms and Networks, edited by Dr. Erich Grotewold and Dr. Nathan Springer. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Eukaryotic DNA is packaged into an array of nucleosomes that consist of histone proteins H2A, H2B, H3 and H4 [1,2]. Nucleosomes connect with each other by a linear linker DNA that is associated with linker histone H1 proteins, which contribute to higher order chromatin structures [3]. During transcription, transcription factors and RNA polymerases must overcome the barriers formed by nucleosomes to get access to DNA for transcription initiation and elongation. Therefore, the positioning and assembly/disassembly of nucleosomes need to be dynamically regulated in the process of transcription [4,5]. This dynamics of nucleosome property is mediated by several distinct but linked mechanisms, including post-translational modification of histones, ATP-dependent sliding or eviction of nucleosomes across the DNA, and exchange of histone variants. Histone variants are related protein isoforms encoded by paralogous genes in each histone class and are distinguished from each other by specific amino acid sequences. In addition to the sequence divergence that may modify nucleosome properties, histone variants often differ by their timing of incorporation into chromatin. For instance, canonical histones are mainly expressed during the S phase of the cell cycle and incorporated into the newly replicated genome. In contrast, other variants are expressed throughout the cell cycle and could be exchanged against canonical histones when nucleosomes are disrupted (e.g. during transcription). These features enable histone variants to shape the chromatin landscapes and decorate regions with divergent transcriptional activities across the genome [6,7]. ☆ This article is part of a Special Issue entitled: Plant Gene Regulatory Mechanisms and Networks, edited by Dr. Erich Grotewold and Dr. Nathan Springer. ⁎ Corresponding author. E-mail address: [email protected] (F. Berger).

In vitro, strong electrostatic interactions between positively charged histones and the negatively charged DNA cause spontaneous, nonspecific aggregates. Histone chaperones facilitate incorporation of histones on DNA by neutralizing their positive charges, and thus play key roles in regulating nucleosome assembly [8]. Nucleosomes are assembled via a stepwise process. First, the H3–H4 tetramer is deposited on DNA, followed by the addition of two flanking H2A–H2B dimers [9]. This process is reversible to allow disassembly of nucleosomes. Histone chaperones comprise a group of complexes containing much diversified proteins that interact either with H2A–H2B or H3–H4 specifically. Moreover, some chaperones exhibit selective binding to certain histone variants. However, the interaction between histone variants and chaperones are not always exclusive [10]. Histone chaperones modulate the dynamics of histone variants deposition into the genome in the right place and at the right time, contributing to the functions of histone variants in chromatin regulation. Here we review recent advances of histone variants in plants, focusing on their function in transcriptional regulation. We describe the properties of histone variants and their chaperones, and highlight their impact in modulating the nucleosome dynamics and chromatin structure. In addition, we discuss recent functional analysis and genome-wide mapping of plant histone variants, their correlation with transcription activity as well as the mechanisms of histone variants in regulating transcription.

2. Core histone variants and chaperones in plants In general, core histone families H2A, and H3 comprise variants, while members of H4 family share exact same amino acid sequence and to date only a few variants have been described from the H2B family in mammals [11,12] and in plants [13].

http://dx.doi.org/10.1016/j.bbagrm.2016.07.002 1874-9399/© 2016 Elsevier B.V. All rights reserved.

Please cite this article as: D. Jiang, F. Berger, Histone variants in plant transcriptional regulation, Biochim. Biophys. Acta (2016), http://dx.doi.org/ 10.1016/j.bbagrm.2016.07.002

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Although they evolved independently in animals and plants, plants H2A and H3 variants acquired very similar specialized features as their counterparts in animals, suggesting evolutionary convergence. The Arabidopsis genome encodes four major types of H2A variants. Among them, canonical H2A, H2A.X and H2A.Z are variants found both in animals and plants. In contrast, H2A.W is a class of variants restricted to the plant kingdom. H2A variants have many amino acids differences across the length of the protein and particularly differ from each other by feature sequences at three regions, the L1 loop, the docking domain and the C-terminal tail (Fig. 1A) [14]. Amino acids in these three regions mediate H2A interaction with other histones within both the same

nucleosome and the neighboring nucleosomes, and thus influence the stability and compaction of nucleosomes [14]. The H3 family consists of three major types of variants, H3.1, H3.3 and CenH3 (Fig. 1B). CenH3 is highly divergent from other H3 variants especially at its N-terminal tail [15,16]. It is deposited specifically at centromeres and is essential for the assembly of kinetochore and correct chromosome segregation during nuclear division [17,18]. Arabidopsis H3.1 and H3.3 variants exhibit only four different amino acids at the positions 31, 41, 87 and 90. Studies of H3.3 deposition at rDNA loci suggested that amino acids 87 and 90 in the core domain of H3.3 guide assembly of H3.3 into the nucleosome, whereas amino acids 31

Fig. 1. Sequence characteristics of main H2A, H3 and H1 variants in Arabidopsis. (A) Sequence alignment of H2A variants. Amino acids in the L1 loop, docking domain and C-terminal regions are indicated by brackets. Canonical H2A and H2A.X variants share common sequences at the L1 loop and docking domain but are distinguished from each other at C-terminal tails, such that canonical H2A ends with a cluster of acidic amino acids; while H2A.X C-terminal harbors conserved SQEF motif that is crucial for H2A.X function in modulating DNA repair, as the serine is phosphorylated at the sites of DNA breaks when DNA damage occurs. Both H2A.Z and H2A.W variants contain unique sequences at the L1 loop, the docking domain and the C-terminal tail. The distinct sequences in the docking domain of H2A.Z are critical for its specific deposition into and exchange from the nucleosome. The C-terminal KSPKK motif of H2A.W may facilitate the formation of higher-order chromatin structures. (B) Sequence alignment of H3.1, H3.3, H3.10 and CenH3. Different Amino acids between H3.1 and H3.3 variants are marked by asterisks. (C) Sequence alignment of linker histone H1 variants. Conserved globular domain is underlined.

Please cite this article as: D. Jiang, F. Berger, Histone variants in plant transcriptional regulation, Biochim. Biophys. Acta (2016), http://dx.doi.org/ 10.1016/j.bbagrm.2016.07.002

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and 41 in the N-terminal tail of H3.3 guide nucleosome disassembly in rDNA loci [19]. The amino acids differences also create biased histone modifications between H3.1 and H3.3 [20,21], influencing the interplay between histone variants and histone modifications. Besides deviations in amino acids, H3.1 and H3.3 are incorporated into chromatin by distinct mechanisms. H3.1 variant is predominantly deposited during the S phase when DNA is replicated, while H3.3 can be incorporated into the nucleosome throughout the cell cycle regardless of DNA synthesis [7,22]. In addition to these three major types of H3 variants, plants also contain additional H3 variants that may play specific functions in regulating chromatin structure and transcription [23,24]. In Arabidopsis, H3 variant H3.10 (also known as MALE GAMETE-SPECIFIC HISTONE3, MGH3) is specifically and abundantly accumulated in sperm cell chromatin and rapidly removed from the zygote after fertilization, indicating a potential role of H3.10 in reprogramming the sperm cell chromatin [25–27]. H3.10 differs from conventional H3.1 and H3.3 variants by many amino acid substitutions especially at its N-terminal tail that is usually subject to various histone modifications (Fig. 1B). These substitutions may block some histone modification sites and meanwhile create new sites for modifications, and thus might facilitate transcriptional reprogramming of chromatin in sperm cell [28]. Like histone variants, most of the histone chaperones are conserved among eukaryotes and several of them are characterized in Arabidopsis (Table 1). Incorporation of H2A.Z requires the ATP-dependent chromatin-remodeling complex SWR1 that partially disassembles the nucleosome to replace H2A–H2B by H2A.Z–H2B dimers [29]. Arabidopsis homologs of SWR1 complex components interact with H2A.Z and are required for H2A.Z incorporation, indicating a conserved function of SWR1 complex in Arabidopsis [30–32]. H2A.Z deposition on the genome is dynamically regulated. In yeast, the incorporated H2A.Z at promoter regions of transcriptional induced genes can be actively removed by SWR1-related INO80 complex [33,34]. Recombinant fragments of Arabidopsis INO80 preferentially bind with H2A.Z–H2B dimers over canonical H2A–H2B dimers [35], suggesting conserved function of INO80 in chaperoning H2A.Z. However, Arabidopsis INO80 is required for H2A.Z incorporation rather than eviction at the 3′ end of some flowering time genes [35]. It remains to investigate how INO80 complex regulates H2A.Z deposition at other regions of Arabidopsis genome. The complex Facilitates Chromatin Transcription (FACT) interacts with H2A–H2B dimers and acts as a transcription elongation factor to assist RNA polymerase II (RNAPII) elongation along the in vitro assembled chromatin template [36,37]. In human and yeast, FACT complex facilitates transcription by evicting H2A–H2B dimers to disassemble nucleosomes or reorganizing the nucleosome structure to increase the accessibility of nucleosomal DNA, without loss of H2A–H2B dimers [38–40]. In maize, the FACT complex subunit Structure-Specific Recognition Protein I (SSRP1) binds with mono-nucleosome particles and is enriched in the highly-nuclease-sensitive fraction of chromatin, which is likely to be transcriptionally competent [41]. Consistent with this Table 1 Summary of Arabidopsis H2A, H3, H1 variants and their potential chaperones. Type

Variants

Chaperones

H2A

Canonical H2A H2A.X H2A.Z H2A.W CenH3 H3.1 H3.3 Other H3 variants H1.1 H1.2 H1.3

NAP1, NRP, FACT FACT SWR1, INO80, Chz1, NAP1, FACT N.D. N.D. CAF1 HIRA, ATRX, DEK N.D. N.D. N.D. N.D.

H3

H1

Chaperones of some variants may only be characterized in non-plant species, and their homologs are presented in plants. N.D., not determined.

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observation, Arabidopsis FACT complex components associate with entire transcribed regions of actively transcribed genes, while it does not occupy transcriptionally inactive regions, supporting its function in transcription elongation through plant chromatin [42]. Besides eviction or destabilization of H2A–H2B dimers for promoting transcription, in yeast and human the FACT complex also mediates deposition and removal of H2A.Z and H2A.X [43,44], adding to the complexity of its function. Other conserved H2A–H2B chaperones in plants include Chz1, Nucleosome Assembly Protein 1 (NAP1) and NAP1-related protein (NRP). In yeast, both Chz1 and NAP1 have been shown to deliver H2A.Z to SWR1 complex for H2A replacement in chromatin [45]. Function of Chz1 in Arabidopsis has not yet been characterized. In addition, although studies on Arabidopsis NAP1 and NRP mutants have revealed their important functions in stress response and plant development [46–50], their chaperone activity to Arabidopsis H2A variants remains to be demonstrated. In mammals, DNA synthesis-dependent deposition of H3.1 is mediated by Chromatin Assembly Factor 1 (CAF1) complex that includes P150, P60, and P48 subunits [51,52]. CAF1 complex is recruited to the DNA synthesis site through its interaction with Proliferating Cell Nuclear Antigen (PCNA) during DNA replication or repair [53–55]. FASCIATA 1 (FAS1), FASCIATA 2 (FAS2) and Multicopy Suppressor of IRA1 (MSI1) are conserved subunits of CAF1 complex in Arabidopsis [56,57]. Loss of CAF1 components perturbs chromatin organization and causes pleiotropic phenotypes during Arabidopsis development and response to genotoxic stress [57–64]. Deposition of Arabidopsis H3.3 is mediated at least by Histone regulator A (HIRA) complex that contains HIRA, Ubinuclein (UBN) 1 and 2, and Calclneurin Binding Protein 1 (CABIN1) [65]. HIRA colocalizes and interacts with H3.3 and other HIRA complex subunits in Arabidopsis [65]. Interestingly, although the HIRA complex is essential for fertilization and early embryogenesis in animals, loss of function of HIRA complex subunits in Arabidopsis only causes mild defects during vegetative development without affecting fertilization and early embryogenesis [65]. It is likely that H3.3 is redundantly deposited by Arabidopsis orthologs of other H3.3 chaperones such as Death-Domain Associated Protein (Daxx), Alpha Thalassemia/ Mental Retardation Syndrome X-Linked (ATRX) and DEK [66–68]. Daxx seems not conserved in plants but Arabidopsis genome encodes both ATRX and DEK homologs. A recent study has revealed that DEK3, one of the four DEK proteins in Arabidopsis, specifically interacts with H3–H4 dimer and regulates nucleosome occupancy, gene expression and stress tolerance [69]. The enrichment of DEK3 at the up- and downstream regulatory gene regions resembles that of histone H3.3 and RNAPII in Arabidopsis and animals [69], supporting a possible role of DEK as H3.3 chaperone in Arabidopsis. 3. Histone variants and heterochromatin silencing Chromatin is organized into transcriptionally active euchromatin and inactive compact heterochromatin. Most of the genes are localized at euchromatin regions, while heterochromatin regions are enriched with transposable elements (TEs) that are usually transcriptional silenced during vegetative development by DNA methylation and histone H3 lysine 9 di-methylation (H3K9me2, a hallmark of heterochromatin) [70,71]. Euchromatin and heterochromatin regions are marked by different histone variants (Fig. 2A), which contribute and indicate their distinct transcriptional activities. The plant specific H2A variant H2A.W is strongly enriched at heterochromatin, TEs and regions enriched in H3K9me2 [70,72]. In addition, H2A.W is strongly depleted from gene bodies and euchromatin regions [72]. Interestingly, although H2A.W is essential and sufficient for the condensation of heterochromatin, loss of H2A.W does not cause a significant derepression of TEs. This is likely due to CHG methylation, which plays a compensatory role in maintaining the repression of TEs. Therefore, H2A.W likely acts in conjunction with DNA methylation to silence the expression of TEs [72]. In vitro nucleosomal arrays demonstrated that H2A.W promotes long-

Please cite this article as: D. Jiang, F. Berger, Histone variants in plant transcriptional regulation, Biochim. Biophys. Acta (2016), http://dx.doi.org/ 10.1016/j.bbagrm.2016.07.002

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Fig. 2. Localization of histone variants across the genome, in TEs and genes. (A) Due to different properties of histone variants, they often preferentially localize at certain chromatin regions including centromere, pericentromeric heterochromatin, euchromatin and telomere. (B) Enrichment of some histone variants defines and represents transcriptional status of TEs and genes. The presence of histone variants at different regions of genes (e.g. TSS, gene body, TTS) may influence transcriptional activity differently.

range nucleosome-nucleosome interactions through its C-terminal tail that contains the conserved KSPKK motif, supporting a role of H2A.W in mediating large-scale chromatin condensation at heterochromatin [72]. Motifs similar to KSPKK are also presented in linker histone H1 and linker region of the vertebrate-specific macroH2A. MacroH2A is concentrated at the inactive X chromosome and is linked to transcriptional repression, and its linker region promotes chromatin condensation [73–75]. This suggests that similar mechanisms may be employed to regulate higher-order heterochromatin formation across eukaryotes. H3.1 is enriched at both H3K9me2 marked regions and H3 lysine 27 tri-methylation (H3K27me3, a euchromatic repressive mark) regions [76,77]. These findings support the view that H3.1 is associated with transcriptional repressed regions both in heterochromatin and euchromatin. Accordingly, a few TEs are transcriptionally derepressed in mutants deprived of CAF1 complex [64,78], presumably because of insufficient H3.1 deposition. Nevertheless, derepression of TEs is moderate and most of the TEs tested are not constantly activated in fas1 and fas2 mutants [64,78], this could be due to the compensation of the loss of H3.1 deposition by other histone chaperones or to activation of a parallel silencing pathway that represses the expression of TEs in the absence of H3.1 deposition. Interestingly, hypermethylated sites with CHG methylation are detected in fas2 mutant [79], suggesting that like H2A.W, H3.1 may also interact with DNA methylation to maintain the repression of TEs. The role played by H3.1 in repression of TEs does not only depend on its preferential deposition at heterochromatin. H3.1 but not H3.3 is a preferred substrate of the SET domain H3K27 methyltransferases ARABIDOPSIS TRITHORAX-RELATED PROTEIN 5 (ATXR5) and ATXR6 [20]. These two enzymes catalyze histone H3 lysine 27 monomethylation (H3K27me1), which is crucial for transcriptional silencing of TEs [80–82]. H3.3 is discriminated by ATXR5 and ATXR6 because the threonine at position 31 (Thr31) of H3.3 inhibits the activity of ATXR5 and ATXR6, while the Alanine at position 31 (Ala31) of H3.1 does not [20]. Replacement of Ala31 to Thr31 in H3.1 protein perturbs the deposition of H3K27me1, accompanied by reactivation of a DNA repeat (TRANSCRIPTIONALLY SILENT INFORMATION-TSI) localized in heterochromatin, demonstrating the importance of Ala31 for the ATXR5 and ATXR6 activity [20]. Escape of H3.3 from being methylated by

ATXR5 and ATXR6 may contribute to the protection of transcriptional active regions occupied by H3.3 against silencing. 4. H2A.Z variant in transcriptional regulation As one of the most conserved histone variants, H2A.Z variant has been extensively studied in yeast, animals and plants, and a strong connection between H2A.Z and transcriptional modulation is established. In Arabidopsis, H2A.Z predominantly associates with genes at euchromatic regions (Fig. 2A) [72,83,84]. At moderately and highly expressed gene loci, H2A.Z is strongly enriched around the nucleosome-depleted region (NDR) at transcriptional start sites (TSSs) particularly within the nucleosome immediately downstream of the TSS (+1 nucleosome) [72,83,84] (Fig. 2B). The +1 nucleosome can act as a major barrier to transcriptional elongation by blocking and stalling RNAPII at essentially all genes [85,86]. In Drosophila, enrichment of H2A.Z at the +1 nucleosome anti-correlates with + 1 nucleosome occupancy and RNAPII stalling [86]. H2A.Z incorporation reduces the height of nucleosomal barriers to RNAPII progression probably by facilitating the loss of H2A.Z/H2B dimer from nucleosome when encountered by RNAPII [86]. Therefore accumulation of H2A.Z around TSSs promotes transcriptional elongation. One of the well-studied Arabidopsis genes that require H2A.Z for their transcription activation is the FLOWERING LOCUS C (FLC). FLC encodes a MADS-box transcription factor that quantitatively represses the floral transition [87,88]. FLC is moderately expressed in rapid-cycling (early-flowering) Arabidopsis accessions such as Columbia (Col). The TSS of FLC locus is enriched with H2A.Z and functional disruption of SWR1 complex compromises H2A.Z deposition at TSS of FLC locus, leading to FLC suppression [30,31,89]. Consistently, reduction of H2A.Z levels also causes FLC repression [30,32]. In Arabidopsis winter annuals, FLC expression is strongly upregulated by a functional FRIGIDA (FRI) allele that confers a requirement for vernalization, a prolonged exposure to cold (a typical winter), to accelerate flowering [90]. FRI acts as a scaffold protein in a transcription activator complex that binds to FLC locus and directly associates with SWR1 complex [91], suggesting that FLC upregulation is mediated by direct modulation of H2A.Z deposition by FRI. Interestingly, H2A.Z accumulation at FLC is not affected when FLC expression is repressed by vernalization [92]. Therefore, H2A.Z at TSS

Please cite this article as: D. Jiang, F. Berger, Histone variants in plant transcriptional regulation, Biochim. Biophys. Acta (2016), http://dx.doi.org/ 10.1016/j.bbagrm.2016.07.002

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may not directly promote transcription but rather configure the chromatin structure competent for transcription by transcriptional activators and machineries. Many Arabidopsis genes also bear high levels of H2A.Z within gene bodies (Fig. 2B) [72,83]. The enrichment of H2A.Z within gene bodies is negatively correlated with gene expression levels [83]. Notably, strong gene body enrichment in H2A.Z represses hypervariable responsive genes that are transcriptionally activated by biotic or abiotic signals [83]. For example, disruption of SWR1 complex induces misexpression of genes that are normally responsive to high temperature in wild type plants [93], genes related to salicylic acid-dependent immune response [32] and phosphate starvation response genes [94]. H2A.Z also impacts on the sensitivity to increased temperature during grain development in Brachypodium [95]. The degree of gene misregulation in h2a.z mutant positively correlates with levels of gene responsiveness and H2A.Z enrichment within gene body [83]. These observations indicate a general role of H2A.Z in regulating responsive genes, rather than modulating gene expression in a specific response group. Genome-wide deposition of H2A.Z is dynamically regulated when the somatic-to–reproductive cell fate transition occurs in Arabidopsis. During the formation of spore mother cells (SMC) in both male and female floral organs, H2A.Z is transiently evicted from the SMC chromatin [96,97]. The eviction of H2A.Z is accompanied by large scale chromatin reprogramming including chromatin decondensation, changes of histone modifications and reduced transcriptional activity [97]. Dynamic incorporation of H2A.Z in SMC may help to establish a distinct chromatin and transcriptional status, which contribute to the differentiation of SMC from its surrounding somatic niche. 5. H3.3 localization in the genome and its implication in transcriptional modulation Subcellular localization studies of GFP-tagged H3.1 and H3.3 proteins in Arabidopsis have demonstrated that unlike H3.1 that is distributed at both pericentromeric heterochromatin (chromocenters) and euchromatin. H3.3 is relatively deprived at chromocenters and enriched at the euchromatin regions [19,26]. Genome-wide profiles of H3.3 confirm the predominant localization of H3.3 at euchromatin (Fig. 2A) [76,98]. H3.3 is enriched at actively transcribed genes; particularly peaks around the transcription termination sites (TTSs) and the levels of H3.3 enrichment at the TTS of genes positively correlate with gene expression (Fig. 2B) [76,98]. H3.3 enriched regions are also marked by active histone modifications such as histone H3 lysine 4 mono-methylation (H3K4me1) and histone H2B mono-ubiquitination (H2Bub) [76,99]. The localization pattern of H3.3 at genes correlates with that of RNAPII, which also peaks towards the TTS of the genes [76,98,100]. It is likely that as a replacement histone, H3.3 is assembled into the nucleosome after the passage of elongating RNAPII, which actively disrupts nucleosomes during transcription. The biological significance of H3.3 deposition in Arabidopsis transcriptional regulation has been studied by investigating the mutant deficient in the H3.3 chaperone HIRA. More than one thousand genes are misregulated in hira mutant. Upregulated genes in hira mutant do not define a specific type of function, suggesting indirect effects from hira mutation. In contrast, a significant number of genes in response to biotic and abiotic stimulus are downregulated upon the loss of HIRA [65]. Accordingly, a significant proportion of downregulated genes are responsive genes enriched with H2A.Z [65]. H2A.Z and H3.3 profiles are anti-correlated, [76]. Whether incorporation of H3.3 on the genome antagonize H2A.Z deposition and vice versa remains to be demonstrated. In animals, H3.3 expression is often induced in various stages of differentiation, and the profiles of H3.3 at developmentally regulated loci change with cellular differentiation [101,102]. In Arabidopsis, dynamics of H3.3 enrichment during leaf formation was investigated using two types of tissues; one contains shoot apical meristem (SAM) and leaf primordia, the other contains mature leaves [98]. Mature leaves are

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formed from leaf primordial that continuously arise from the SAM. It revealed that transcriptional changes during the developmental transition from SAM and leaf primordial to mature leaves are closely accompanied with changes of H3.3 enrichment. Transcriptional repression is associated with a strong reduction of H3.3 levels around the TTS of genes, while transcriptional activation is coupled with an enhancement of H3.3 signals at the TTS. This dynamic replacement of H3.3 suggests a function of H3.3 in establishing new expression programs during development and differentiation probably by facilitating global changes of chromatin structure and histone modifications [98]. Similarly, the likely deprivation of H3.3 deposition in hira mutant protoplasts prevents the mis-expression of a significant number of genes that changes during wild type protoplasts induction and hira mutant is deficient in regeneration, suggesting that HIRA mediated H3.3 deposition participates in reprogramming transcription during dedifferentiation of plant cells [65]. In Arabidopsis, H3.3 also associates with promoter regions, though at lower levels [103]. In contrast to TSS enriched H3.3 that often reflects high transcription, genes that carry H3.3 only at promoters exhibit low expression levels and are subject to strong transcriptional regulation. In addition, genes with promoters enriched in H3.3 tend to associate with higher H3K27me3 over gene body then other inactive genes [103]. In mammalian embryonic stem cell, H3.3 deposited by HIRA facilitates recruitment of a conserved complex Polycomb Repressive Complex 2 (PRC2), which deposits H3K27me3 in both animals and plants [104]. It is not clear whether H3.3 enrichment at promoters in Arabidopsis plays a similar function for PRC2 recruitment at downstream genes. In animals, H3.3 is also deposited at pericentromeric heterochromatin regions and heterochromatic telomeres, mediated by Daxx and ATRX, which contribute to the repression of telomeric repeats [67,101, 105]. These findings suggest that H3.3 may function in transcriptional silencing. A detailed analysis focused on repetitive regions at Arabidopsis centromeres and telomeres using H3.1 and H3.3 genome-wide mapping data [76,98] suggested that centromeric repeats are enriched with H3.1, while telomeres are enriched with H3.3 [106] (Fig. 2A). The presence of Arabidopsis H3.3 at telomeres is in line with the observations that Arabidopsis telomeres exhibit euchromatic features [107]. However, enrichment of Arabidopsis H3.3 at pericentromeric heterochromatin regions is deficient through not completely depleted. In addition, the presence of a conserved pathway that deposits H3.3 into pericentromeric heterochromatin is obscure in Arabidopsis, as Daxx is not conserved in plants and the function of ATRX is not characterized yet. A recent study reported that some TEs are derepressed in Arabidopsis hira mutant [108], but its link with H3.3 function awaits further clarification. 6. Stress induced histone H1 variant and its potential roles in stress related transcriptional regulation By binding to the linker DNA segments entering and exiting the nucleosome core particle, the linker H1 histones play important roles in establishing and maintaining higher order chromatin structure, and thus restrict DNA accessibility. H1 proteins are variable at N-terminal and C-terminal tails, while the central globular domain is generally conserved [109]. Although recent studies have started to reveal functional specificity of H1 variants in different organisms, it is not clear whether H1 variants belong to distinct functional subgroups. Arabidopsis genome encodes three H1 variants: ubiquitously expressed H1.1, H1.2 and stress inducible H1.3 that is significantly shorter than the other two H1 proteins (Fig. 1C) [110]. This stress inducible H1 variant is evolutionary conserved among plant species, and the expression of its relatives in other plant species is also induced by stress conditions such as drought stress and exposure to abscisic acid (ABA) [111–114]. Knockdown of stress inducible H1 variant in tomato exhibits increased stomatal conductance, transpiration and photosynthetic rate, suggesting a role in the regulation of stomata [115]. Without stress induction, Arabidopsis

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H1.3 is restricted in guard cells and is required for stomata development and function [116]. Under stress conditions, H1.3 expression is induced and expands to other cell types. Loss of H1.3 decreases the plant response ability to combined low light and drought stress and impairs the transcriptional reprogramming under stress conditions. Compare with the other two H1 variants, H1.3 prefers to bind more transcriptional active chromatin and association of H1.3 with chromatin is more dynamic, suggesting specific properties associated with H1.3. H1.3 may mediate stress related transcriptome change by facilitating DNA hypermethylation, as in h1.3 mutant stress induced DNA hypermethylation is significantly decreased [116]. It has been demonstrated that H1.1 and H1.2 block the access of DNA methyltransferases to DNA [117]. H1.3 may compete with H1.1 and H1.2 under stress conditions, and thus interference the DNA accessibility to DNA methyltransferases. 7. Conclusions and future directions Chromatin regulation of transcription acts through mediating DNA exposure to transcriptional machineries. Exchange of histone variants alters the stability and dynamics of nucleosomes and thus modulates DNA accessibility. Incorporation of histone variants is not the only mechanism that impacts on the chromatin structure. Histone variants likely coordinate with histone modifications and chromatin remodeling to regulate nucleosome properties and transcription. Moreover, different histone variants may act as distinct platforms to attract specific transacting factors, which function differently in transcriptional regulation. Developmental transitions are usually coupled with extensive change of chromatin features and transcriptional program. In addition, as sessile organisms, plants have to adjust chromatin and transcription rapidly to cope with the environmental fluctuation and unexpected abiotic stress in order to adapt and survive. Genome wide turnover of histone variants provides an efficient and rapid way to fundamentally reset the chromatin landscape and transcription. Current studies in plants provide clues for the possible roles of histone variants in developmental transitions and stress response but the mechanisms involved remain unclear. Currently the functional dissection of histone variants and other chromatin regulatory factors in plants has been hampered by widespread use of whole tissues containing multiple cell types for chromatin profiling. It is becoming apparent that different cell types have distinct chromatin and transcriptional characteristics that reflect their specific developmental status and capacity to respond to environmental stimuli. Utilization of single cell types for chromatin characterization will help to elucidate the epigenetic reprogramming during cell differentiation and environmental response. Acknowledgments Danhua Jiang is supported by an EMBO Long-Term Fellowship (ALTF 1129-2013). F. Berger Laboratory is funded by the Austrian Academy of Sciences, and FWF (grant number P 27535-B21) and supported by Gregor Mendel Institute at Vienna Biocenter. The authors DJ and FB declare no conflict of interest related to this work. References [1] K. Luger, A.W. Mader, R.K. Richmond, D.F. Sargent, T.J. Richmond, Crystal structure of the nucleosome core particle at 2.8 A resolution, Nature 389 (1997) 251–260. [2] R.D. Kornberg, Chromatin structure: a repeating unit of histones and DNA, Science 184 (1974) 868–871. [3] S.W. Harshman, N.L. Young, M.R. Parthun, M.A. Freitas, H1 histones: current perspectives and challenges, Nucleic Acids Res. 41 (2013) 9593–9609. [4] M. Radman-Livaja, O.J. Rando, Nucleosome positioning: how is it established, and why does it matter? Dev. Biol. 339 (2010) 258–266. [5] S. Venkatesh, J.L. Workman, Histone exchange, chromatin structure and the regulation of transcription, Nat. Rev. Mol. Cell Biol. 16 (2015) 178–189. [6] C.M. Weber, S. Henikoff, Histone variants: dynamic punctuation in transcription, Genes Dev. 28 (2014) 672–682.

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Please cite this article as: D. Jiang, F. Berger, Histone variants in plant transcriptional regulation, Biochim. Biophys. Acta (2016), http://dx.doi.org/ 10.1016/j.bbagrm.2016.07.002