Available online at www.sciencedirect.com Current Opinion in ScienceDirect Plant Biology Illuminating the Arabidopsis circadian epigenome: Dynamics of histone acetylation and deacetylation Lu Xiong1,a, Wenguan Zhou1,a and Paloma Mas1,2 Abstract in synchrony with the environmental time. The main The circadian clock generates rhythms in biological processes output of the circadian function is the generation of 24- including plant development and metabolism. Light synchronizes h biological rhythms precisely timed to occur at the the circadian clock with the day and night cycle and also triggers most favorable daily or seasonal time [1]. Consistently, developmental transitions such as germination, or flowering. The the circadian function has been proposed to improve circadian and light signaling pathways are closely interconnected fitness and survival, providing an adaptive advantage [2]. and understanding their mechanisms of action and regulation The importance of the circadian function in plants is requires the integration of both pathways in their complexity. Here, also manifested by the plethora of processes regulated we provide a glimpse into how chromatin remodeling lies at the by the clock, including among others, physiological re- interface of the circadian and light signaling regulation. We focus sponses, metabolic homeostasis or cellular growth and on histone acetylation/deacetylation and the generation of development [1e4]. Generation of rhythms relies on permissive or repressive states for transcription. Several chro- the proper perception of environmental cues that set matin remodelers intervene in both pathways, suggesting that the time-of-day [5], and the delicate cross-regulation interaction with specific transcription factors might specify the among oscillator components that ultimately generate proper timing or light-dependent responses. Deciphering the rhythmic oscillations in the output processes regulated repertoire of chromatin remodelers and their interacting tran- by the clock [1]. scription factors will provide a view on the circadian and light- dependent epigenetic landscape amenable for mechanistic The main oscillator components in Arabidopsis thaliana studies and timely regulation of transcription in plants. display sequential peaks of expression and activity during the day or night (Figure 1). For instance, clock Addresses components acting during the day include the single 1 Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA- MYB transcription factors CIRCADIAN CLOCK UAB-UB, Campus UAB, Bellaterra, 08193, Barcelona, Spain 2 Consejo Superior de Investigaciones Científicas (CSIC), 08028, ASSOCIATED1 (CCA1) and LATE ELONGATED Barcelona, Spain HYPOCOTYL (LHY) and the morning-expressed Pseudo-Response Regulators PRR9 and PRR7 [1,6], Corresponding author: Mas, Paloma (paloma.mas@cragenomica.es) which act mainly as transcriptional repressors. Other a Contributed equally to this work. morning-expressed components that function as acti- vators include the REVEILLE (RVE) protein family Current Opinion in Plant Biology 2022, 69:102268 and NIGHT LIGHT-INDUCIBLE AND CLOCK- This review comes from a themed issue on Epigenetics and gene REGULATED GENES (LNKs). Later during the day regulation (2022) and close to dusk, PRR5 and TIMING OF CAB Edited by Dr. Bob Schmitz and Dr. Ortrun Mittelsten Scheid EXPRESSION1 (TOC1/PRR1) exert a repressive function [1,6] that is temporally followed by the ac- For complete overview of the section, please refer the article collection - Epigenetics and gene regulation (2022) tivity of EARLY FLOWERING 3 (ELF3), ELF4 and LUX ARRHYTHMO/PHYTOCLOCK1 (LUX/PCL1), Available online 31 July 2022 which assemble into the Evening Complex (EC) to https://doi.org/10.1016/j.pbi.2022.102268 repress gene expression during the night [7]. Overall, 1369-5266/© 2022 The Authors. Published by Elsevier Ltd. This is an multiple regulatory mechanisms are responsible for the open access ar ticle under the CC BY-NC-ND license (http:// regulation of rhythmic gene and protein expression and creativecommons.org/licenses/by-nc-nd/4.0/). activity. The mechanisms pervade different stages of transcriptional and translational regulation [6,8,9]. The Keywords past years has also seen an increase in our under- Circadian clock, Light signaling, Histone acetylation, Histone deacety- standing on the connection between the circadian lation, Arabidopsis thaliana. function and changes in chromatin remodeling [10]. Introduction Post-translational modifications of histones are one of the Plants, as many other organisms, use a cellular mecha- well-studied mechanisms associated with transcriptional nism or circadian clock to coordinate biological processes regulation [11]. The link of these modifications with www.sciencedirect.com Current Opinion in Plant Biology 2022, 69:102268 2 Epigenetics and gene regulation (2022) Figure 1 Simplified transcriptional regulatory network at the core of the Arabidopsis circadian clock. The expression and function of the main oscillator components occur at specific times during the day and night. Most of the components act as repressors of oscillator gene expression (red lines) although some components have been described as activators (blue lines). Tripartite protein complex known as the Evening Complex (EC) is delimited by the dotted line. Please consult the text for further details. transcriptional regulation relies on particular histone ELONGATED HYPOCOTYL3 (FHY3) [16]. Thus, modifications favoring chromatin conformation changes an intricate balance between photoreceptors and COP1 that result in permissive or repressive chromatin states signaling cascades under light and dark conditions de- and thus affecting the transcriptional machinery acces- fines the photomorphogenesis or skotomorphogenesis sibility and transcription factor binding [12]. Histone reprogramming, respectively. acetylation is one of the well-studied histone modifica- tions correlated with gene activation. Acetylation relies The circadian system and light signaling pathways on the activities of histone acetyltransferases (HATs) regulate each other, shared molecular components and that ensure chromatin commitment for inducible gene regulatory mechanisms. One of the shared regulatory activation. The HAT activities are dynamically counter- mechanisms is the changes in chromatin conformation balanced by histone deacetylases (HDACs), which favor and its correlation with transcriptional regulation deacetylation and gene repression. The correlation be- [10,17]. In this review, we provide a glimpse of the tween rhythmic changes in gene expression with oscil- commonalities and divergences of the epigenetic regu- latory chromatin conformations and histone acetylation lation of clock- and light-related signaling pathways, has been previously established [10]. Several studies with particular emphasis on histone acetylation and have also identified the chromatin-related factors deacetylation. We briefly describe circadian and light- contributing to these rhythmic oscillations [10]. mediated regulatory changes in chromatin status and the chromatin remodelers involved in such regulations. Light is one of the main environmental cues responsible Lessons learnt in one pathway can lead the way for for resetting the clock every day [5]. Light also regulates similar discoveries in the other. many essential aspects of plant growth and development [13]. For instance, upon light perception, photorecep- Circadian and light-dependent changes of tors such as PHYTOCHROMES and CRYPTO- histone acetylation CHROMES initiate complex molecular cascades to Since the first study, nearly 15 years ago, showing that reprogram seedlings for photomorphogenesis [14]. rhythmic changes in Histone 3 (H3) acetylation at the Conversely, under dark conditions, seedlings undergo promoter of a clock gene correlated with the transcrip- skotomorphogenesis characterized by closed cotyledons, tional rhythms of clock gene expression [18], many and elongated hypocotyls. The CONSTITUTIVE other oscillator genes have been shown to be rhythmi- PHOTOMORPHOGENIC1/DEETIOLATED/FUSCA cally decorated with different chromatin marks [10]. (COP1/DET/FUS) E3 ligase complex [15] act as a core The generation of transcriptional rhythms in steady- repressor of photoreceptor signaling cascade by pro- state and nascent RNAs [19], relies on a complex moting in the dark, the proteasome degradation of many interplay between chromatin remodelers and oscillator key transcription factors, including among others components. Rhythmic changes in chromatin rely on the ELONGATED HYPOCOTYL 5 (HY5) or FAR-RED circadian regulation of the expression chromatin-related Current Opinion in Plant Biology 2022, 69:102268 www.sciencedirect.com Chromatin and the plant circadian clock Xiong et al. 3 factors [20], and/or in the direct interaction of oscillator dependent transcriptional regulation is the HISTONE components with chromatin-related factors. These ACETYLTRANSFERASE OF THE TAFII250 FAMILY mechanisms ultimately allow the rhythmic recruitment 2 (HAF2/TAF1). Indeed, a recent study has shown that of the chromatin-related factors to the clock loci [10]. CCA1 controls the expression of HAF2, which activates clock genes expressed close to dusk or during the night The study showing that the raising phase of TOC1 [31]. The same chromatin modifier, HAF2 [32e34], is oscillatory waveform correlated with rhythms in H3 an important activator of light-regulated gene expres- acetylation at the TOC1 promoter [18] was later sion (red/far-red and blue light signals) through histone followed by evidence of oscillatory changes in histone acetylation. Thus, HAF2 regulates both night-expressed acetylation at the promoters of other oscillator genes clock components and light-regulated genes. Eluci- [21e23]. The two morning-expressed single MYB dating the molecular components directing HAF2 to the transcription factors CCA1 and RVE8 were found to light and clock-related target loci might provide clues perform antagonistic functions shaping the circadian into the specificities of this dual regulation. waveform of histone acetylation at the TOC1 promoter. While CCA1 repressed TOC1 and favored histone The histone acetyltransferase GENERAL CONTROL deacetylation [18], RVE8 activated TOC1 expression by NONDEREPRESSIBLE 5 (GCN5) was also proposed to enhancing to histone acetylation [24]. The transcrip- favor acetylation of histone lysine residues and chromatin tionally permissive chromatin conformations favored by commitment for light-dependent up-regulation of gene RVE8 correlated with the rhythmic recruitment of the expression [32,33]. Interestingly, GCN5 and HAF2 were transcriptional machinery through interaction with the both required for sustaining histone acetylation (H3K9, RNA Polymerase II and the FACT complex [19]. How- H3K27, and H4K12) on the target promoters, whereas ever, the chromatin remodelers involved in histone H3K14 acetylation was proposed to rely only on GCN5 acetylation, working in conjunction with RVE8 remain [32]. As GCN5 is associated with a large number of gene to be identified. promoters involved in many different processes [33], it is possible that GCN5 might be involved in the transcrip- Changing light conditions also modulate the pattern of tional regulation of clock genes. If that is the case, GCN5 histone modifications such as acetylation at light- may directly interact with clock proteins to regulate regulated gene loci. This mechanism directly connects circadian gene expression. light with transcriptional regulation [25,26]. Distinct photoreceptors contribute to the effects of the different Recent studies have also shown that the basic helix-loop- light qualities on histone modifications [26]. Notably, helix transcription factors known as PHYTOCHROME- the expression of the photoreceptors themselves seems INTERACTING FACTORs (PIFs) contribute to H3 to be regulated by chromatin remodeling. For instance, acetylation and removal of the histone variant H2A.Z in the up-regulation of the photoreceptor PHYTO- response to changes in light quality [35]. The study CHROME A (PHYA) is associated with an increased shows that the epigenetic function of PIFs relies on the pattern of histone acetylation at the PHYA locus [27]. interaction with EIN6 ENHANCER, the homolog of the Some of the components involved in the regulation of chromatin remodeling complex subunit INO80 Subunit histone acetylation have been reported, including the 6 [35]. Notably, the INO80 complex represses the tran- master repressors of photomorphogenesis COP1 and scription of a central clock gene in Neurospora crassa [36]. DET1, which are involved in the light-dependent con- Thus, future studies could focus on whether the plant trol of gene-specific histone modifications [26]. INO80 complex also contributes to circadian clock gene expression in plants. The connection of COP1 and DET1 with the plant circadian clock has been shown in several studies. For example, COP1 directly interacts with the clock Histone deacetylation and repression of component ELF3 to regulate photoperiodic flowering light- and circadian-regulated genes [28]. Other examples include the interaction of DET1 Several HDACs relate to both the circadian clock and with CCA1 and LHY, which contributes to the tran- light signaling. For instance, the HISTONE DEACE- scriptional repressive function of CCA1 and LHY [29]. TYLASE 1/HISTONE DEACETYLASE 19 (HD1/ Furthermore, COP1 SUPPRESSOR 4 (CS4), a sup- HDA19; herein HDA19) (Figure 2a) interacts with the pressor of the cop1 mutant, also represses CCA1 target clock-related component CCA1 HIKING EXPEDI- genes by directly interacting with CCA1 [30]. Thus, TION (CHE/TCP21) to regulate the morning-expressed COP1 and DET1 interaction with clock components clock gene CCA1 [37]. HD1/HDA19, together with the seems to be important for regulation of clock gene SWI-INDEPENDENT3 LIKE (SNL1 and SNL6), also expression and light-dependent clock outputs. act as a negative regulator of the light signaling pathway by facilitating histone deacetylation of the PHYTO- An example of a chromatin-remodeling factor regulating CHROME A (PHYA) locus [38]. HDA19 regulation of both rhythmic clock gene expression and light- light-dependent gene expression might be achieved by www.sciencedirect.com Current Opinion in Plant Biology 2022, 69:102268 4 Epigenetics and gene regulation (2022) Figure 2 Examples of shared histone deacetylases related to both the circadian clock and light signaling. a) HDA19 interacts with the clock component CHE to regulate CCA1 expression, and with several light-related components in the regulation of light signaling pathways. b) HDA6 interacts with clock proteins and light-signaling components to the circadian clock and light signaling pathways. Red lines denote repression. Please consult the text for further details. counteracting the histone acetylation activities of HAF2 HDA6 has been also connected with light signaling. For and GCN5 [32]. Light-dependent regulation might also instance, natural variation studies identified poly- rely on HDA19 antagonistic function with the photo- morphic alleles of HDA6 and PHYB involved in light- morphogenic transcription factor ELONGATED HY- dependent regulation of chromatin compaction associ- POCOTYL5 (HY5) [38] (Figure 2a). Whether HDA19 ated with acclimation [42]. HDA6 has been associated counteracts HAF2 activity in the regulation of clock with other pathways, such as light-dependent seed genes remains to be identified. germination by carbon monoxide [43] or the light- mediated nitric oxide (NO) signaling [44]. Further- Another HDAC, the HISTONE DEACETYLASE-6 more, HDA6 is recruited by DET1 and FAR-RED (HDA6) forms a protein complex with members of ELONGATED HYPOCOTYL3 (FHY3) to the ABA the Groucho/Tup1 protein family, topless/topless- INSENSITIVE5 (ABI5) locus to contribute to the light- related (TPL/TPR), and with the clock component and ABA-dependent control of seedling greening [45] PRR9 for transcriptional repression of the morning- (Figure 2b). Similar to the circadian system, HDA6 expressed clock genes CCA1 and LHY, most likely by regulates light signaling pathways by interaction with an modulating the pattern of H3 deacetylation [39] array of different photomorphogenic-related compo- (Figure 2b). Molecularly, this regulation appears to be nents. Further studies could focus on the possible role of mediated by HDA6 interaction with the LYSINE- HDA6-LDL1/2 complex in light signaling and its regu- SPECIFIC DEMETHYLASE 1 (LSD1)-LIKE 1/2 lated output pathways. (LDL1/2). The complex is recruited by TOC1 to the clock-related target loci to repress their expression The HISTONE DEACETYLASE 15 (HDA15) is a [40]. In turn, the HDA6-LDL1/2 complex interacts central hub connecting light signaling and chromatin with CCA1 and LHY to repress TOC1 expression [41]. changes at multiple levels (Figure 3). Indeed, HDA15 Thus, HDA6 regulates both morning- and evening- interacts with a number of photomorphogenic-related expressed clock genes by interaction with LDL1/2 components to regulate the pattern of histone acetyla- and with many clock components including PRR9, tion at the target genes. For example, HDA15 represses CCA1, LHY and TOC1 (Figure 2b). gene expression in etiolated seedlings through its Current Opinion in Plant Biology 2022, 69:102268 www.sciencedirect.com Chromatin and the plant circadian clock Xiong et al. 5 interaction with PHYTOCHROME INTERACTING HDA15 subcellular localization and its implication in FACTOR3 (PIF3). Red light represses the binding to the regulation of evening-expressed clock genes. the target loci, providing a mechanism whereby PIF3 and HDA15 repress chlorophyll biosynthetic and The histone deacetylase (HDA9) also contributes to the photosynthetic genes [46]. HDA15 also interacts with repression of many genes by interacting with a wide PIF1 to regulate the expression of light-responsive range of proteins [53] including those involved in light genes involved in seed germination [47]. HDA15 also signaling and the circadian system. Indeed, HDA9 in- directly interacts with HY5 to repress hypocotyl growth teracts with the Evening complex (EC) component under red and far-red light conditions. The HDA15 and EARLY FLOWERING 3 (ELF3) and favors histone HY5 interaction also regulates H4 acetylation of cell- deacetylation at the TOC1 promoter and TOC1 repres- wall and auxin-related genes [48]. sion after dusk [54]. HDA9 also functions synergistically with HY5 within the autophagy pathway, and in HDA15 also controls HY5 and PIFs through its inter- response to light-to-dark transitions and nitrogen star- action with COP1. Indeed, HDA15 modulates COP1 vation [55]. In addition to its role as a repressor favoring repressing function in the regulation of HY5 and PIF3 histone deacetylation, HDA9 can also function in tran- protein abundance in a light-dependent manner. The scriptional activation [53]. authors thus propose that HDA15 positively regulates photomorphogenesis through a post-translational The circadian clock rhythmically regulates the expres- mechanism [49]. It would be interesting to examine sion of some chromatin related components [20]. The whether HDA15 and COP1 are also involved in the biological relevance of such oscillation has been regulation of clock protein abundance. HDA15 regula- demonstrated in studies of the SWI-independent 3/ tory function might be also defined by its subcellular histone deacetylase (Sin3-HDAC) genes SAP30 localization. Indeed, light and dark conditions control FUNCTION-RELATED 1 (AFR1), and AFR2, which are the nucleocytoplasmic shuttling of HDA15: while light expressed in the evening. The AFR proteins bind to the favors HDA15 nuclear accumulation, dark conditions CCA1 and PRR9 gene promoters and repress their trigger HDA15 export out of the nucleus [50]. expression during the night by favoring histone deace- tylation at their promoters [56]. The MADS transcrip- HDA15 also interacts with the Nuclear Factor-YC (NF- tion factor AGAMOUS-like 15 (AGL15) also interacts YC) proteins under light conditions, and represses the with members of the SIN3/HDAC complex providing a expression of hypocotyl elongation-related genes by mechanism whereby AGL15 represses its target genes controlling H4 acetylation at their promoters. Under [57]. It would be interesting to examine whether AFR1 darkness, the HDA15-NF-YC complex dissociates from and AFR2 regulate light signaling pathways by direct the promoters leading to increased H4 acetylation and interaction of photomorphogenic-related components. etiolated growth [51]. Interestingly, the clock compo- nent TOC1 assembles into a protein complex Perspectives comprising NF-YB/C, which recruits HDA15 to repress Light signaling modulates chromatin compaction, het- growth-related gene expression [52]. Further studies are erochromatin reorganization and transcriptional reprog- required to examine in detail the diurnal changes in ramming through processes that are regulated by the Figure 3 HDA15 lies at the interface of light and clock regulated processes. The interaction of HDA15 with light- and clock-related components in the control of several relevant processes including photosynthesis and growth, among others. Red lines denote repression. 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The review describes studies in Arabidopsis and other crops, focusing, among others, on hybrid vigor Funding and epigenetic changes at clock loci and the function of epialleles in The Mas laboratory is funded with a research grant the regulation of output traits during crop domestication. (PID2019-106653GB-I00) from the MCIN/AEI/ 11. Jenuwein T, Allis CD: Translating the histone code. Science 2001, 293:1074–1080. 10.13039/501100011033, from the Ramon Areces Foundation and from the Generalitat de Catalunya 12. Berger SL: The complex language of chromatin regulation during transcription. Nature 2007, 447:407–412. (AGAUR). P.M. laboratory also acknowledges financial support from the CERCA Program/Generalitat de 13. Kami C, Lorrain S, Hornitschek P, Fankhauser C: Light-regu- lated plant growth and development. Curr Top Dev Biol 2010, Catalunya and by the “Severo Ochoa Program for Cen- 91:29–66. ters of Excellence in R&D” (CEX2019-000902-S) 14. Cheng MC, Kathare PK, Paik I, Huq E: Phytochrome signaling funded by MCIN/AEI/10.13039/501100011033. L.X. * * networks. Annu Rev Plant Biol 2021, 72:217–244. and W.Z. are recipients of CSC fellowships funded by This review provides an interesting and comprehensive view about the modular nature of phytochromes, and their molecular counterparts, China Scholarship Council. phytochrome-interacting proteins. The review describe the phytochrome signaling cascades and their influence on several regulatory mecha- nisms including their role in transcriptional control, alternative splicing, Declaration of competing interest and translational regulation in the control of photomorphogenesis. The authors declare that they have no known competing 15. Lau OS, Deng XW: The photomorphogenic repressors COP1 financial interests or personal relationships that could and DET1: 20 years later. Trends Plant Sci 2012, 17:584–593. have appeared to influence the work reported in this 16. 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Zhao L, Peng T, Chen CY, Ji R, Gu D, Li T, Zhang D, Tu YT, * * He Y, Nery JR, Chen H, Chen M, et al.: PHYTOCHROME- * Wu K, Liu X: HY5 interacts with the histone deacetylase INTERACTING FACTORs trigger environmentally responsive HDA15 to repress hypocotyl cell elongation in photomor- chromatin dynamics in plants. Nat Genet 2021, 53:955–961. phogenesis. Plant Physiol 2019, 180:1450–1466. This study provides a molecular mechanism explaining the connection In this study, the authors show that HY5 requires HDA15 for repressing of the histone variant H2A.Z, histone H3 acetylation and PIF activity in hypocotyl cell elongation by modulating histone H4 acetylation in a the control of gene networks regulated by the environmental condi- light-dependent manner. Genome-wide transcriptome studies also tions. The authors show that PIFs modulate H2A.Z and H3K9ac showed that HDA15 and HY5 co-repress the transcription of genes deposition in a process that is controlled by light quality. 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