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Abstract

The basic unit of chromatin, the nucleosome, is an octamer of four core histone proteins (H2A, H2B, H3, and H4) and serves as a fundamental regulatory unit in all DNA-templated processes. The majority of nucleosome assembly occurs during DNA replication when these core histones are produced en masse to accommodate the nascent genome. In addition, there are a number of nonallelic sequence variants of H2A and H3 in particular, known as histone variants, that can be incorporated into nucleosomes in a targeted and replication-independent manner. By virtue of their sequence divergence from the replication-coupled histones, these histone variants can impart unique properties onto the nucleosomes they occupy and thereby influence transcription and epigenetic states, DNA repair, chromosome segregation, and other nuclear processes in ways that profoundly affect plant biology. In this review, we discuss the evolutionary origins of these variants in plants, their known roles in chromatin, and their impacts on plant development and stress responses. We focus on the individual and combined roles of histone variants in transcriptional regulation within euchromatic and heterochromatic genome regions. Finally, we highlight gaps in our understanding of plant variants at the molecular, cellular, and organismal levels, and we propose new directions for study in the field of plant histone variants.

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2022-05-20
2024-10-06
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Literature Cited

  1. 1.
    Andrews AJ, Luger K. 2011. Nucleosome structure(s) and stability: variations on a theme. Annu. Rev. Biophys. 40:99–117
    [Google Scholar]
  2. 2.
    Ascenzi R, Gantt JS. 1997. A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol. Biol. 34:4629–41
    [Google Scholar]
  3. 3.
    Ausió J. 2000. Are linker histones (histone H1) dispensable for survival?. Bioessays 22:10873–77
    [Google Scholar]
  4. 4.
    Bagchi DN, Battenhouse AM, Park D, Iyer VR 2020. The histone variant H2A.Z in yeast is almost exclusively incorporated into the +1 nucleosome in the direction of transcription. Nucleic Acids Res. 48:1157–70
    [Google Scholar]
  5. 5.
    Benoit M, Simon L, Desset S, Duc C, Cotterell S et al. 2019. Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development. New Phytol. 221:1385–98
    [Google Scholar]
  6. 6.
    Berriri S, Gangappa SN, Kumar SV. 2016. SWR1 chromatin-remodeling complex subunits and H2A.Z have non-overlapping functions in immunity and gene regulation in Arabidopsis. Mol. Plant 9:71051–65
    [Google Scholar]
  7. 7.
    Boden SA, Kavanová M, Finnegan EJ, Wigge PA. 2013. Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes. Genome Biol. 14:6R65
    [Google Scholar]
  8. 8.
    Bönisch C, Hake SB. 2012. Histone H2A variants in nucleosomes and chromatin: more or less stable?. Nucleic Acids Res. 40:2110719–41
    [Google Scholar]
  9. 9.
    Borg M, Jiang D, Berger F. 2021. Histone variants take center stage in shaping the epigenome. Curr. Opin. Plant Biol. 61:101991
    [Google Scholar]
  10. 10.
    Bourguet P, Picard CL, Yelagandula R, Pélissier T, Lorković ZJ et al. 2021. The histone variant H2A.W and linker histone H1 co-regulate heterochromatin accessibility and DNA methylation. Nat. Commun. 12:12638
    [Google Scholar]
  11. 11.
    Cai H, Zhang M, Chai M, He Q, Huang X et al. 2019. Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3. New Phytol. 221:1295–308
    [Google Scholar]
  12. 12.
    Carter B, Bishop B, Ho KK, Huang R, Jia W et al. 2018. The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis. Plant Cell 30:61337–52
    [Google Scholar]
  13. 13.
    Charbonnel C, Allain E, Gallego ME, White CI 2011. Kinetic analysis of DNA double-strand break repair pathways in Arabidopsis. DNA Repair 10:6611–19
    [Google Scholar]
  14. 14.
    Choi J, Lyons DB, Kim MY, Moore JD, Zilberman D. 2020. DNA methylation and histone H1 jointly repress transposable elements and aberrant intragenic transcripts. Mol. Cell 77:2310–23.e7
    [Google Scholar]
  15. 15.
    Choi K, Kim S, Kim SY, Kim M, Hyun Y et al. 2005. SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17:102647–60
    [Google Scholar]
  16. 16.
    Choi K, Park C, Lee J, Oh M, Noh B, Lee I 2007. Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134:101931–41
    [Google Scholar]
  17. 17.
    Clarkson MJ, Wells JRE, Gibson F, Saint R, Tremethick DJ. 1999. Regions of variant histone His2AvD required for Drosophila development. Nature 399:6737694–97
    [Google Scholar]
  18. 18.
    Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B et al. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:7184215–19
    [Google Scholar]
  19. 19.
    Cole L, Kurscheid S, Nekrasov M, Domaschenz R, Vera DL et al. 2021. Multiple roles of H2A.Z in regulating promoter chromatin architecture in human cells. Nat. Commun. 12:12524
    [Google Scholar]
  20. 20.
    Coleman-Derr D, Zilberman D. 2012. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLOS Genet. 8:10e1002988First genome-wide correlation of Arabidopsis H2A.Z enrichment in the gene body and transcriptional repression.
    [Google Scholar]
  21. 21.
    Colino-Sanguino Y, Clark SJ, Valdes-Mora F. 2022. The H2A.Z-nucleosome code in mammals: emerging functions. Trends Genet 38:3273–89
    [Google Scholar]
  22. 22.
    Collins PL, Purman C, Porter SI, Nganga V, Saini A et al. 2020. DNA double-strand breaks induce H2Ax phosphorylation domains in a contact-dependent manner. Nat. Commun. 11:13158
    [Google Scholar]
  23. 23.
    Core LJ, Waterfall JJ, Gilchrist DA, Fargo DC, Kwak H et al. 2012. Defining the status of RNA polymerase at promoters. Cell Rep. 2:41025–35
    [Google Scholar]
  24. 24.
    Cortijo S, Charoensawan V, Brestovitsky A, Buning R, Ravarani C et al. 2017. Transcriptional regulation of the ambient temperature response by H2A.Z nucleosomes and HSF1 transcription factors in Arabidopsis. Mol. Plant 10:101258–73
    [Google Scholar]
  25. 25.
    Crevillén P, Gómez-Zambrano Á, López JA, Vázquez J, Piñeiro M, Jarillo JA 2019. Arabidopsis YAF9 histone readers modulate flowering time through NuA4-complex-dependent H4 and H2A.Z histone acetylation at FLC chromatin. New Phytol. 222:41893–908H2A.Z acetylation is observed for the first time in plants and required for FLC expression.
    [Google Scholar]
  26. 26.
    Dai X, Bai Y, Zhao L, Dou X, Liu Y et al. 2017. H2A.Z represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in Arabidopsis. Mol. Plant10(10):1274–92
    [Google Scholar]
  27. 27.
    Dawson MA, Bannister AJ, Göttgens B, Foster SD, Bartke T et al. 2009. JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin. Nature 461:7265819–22
    [Google Scholar]
  28. 28.
    Deal RB, Kandasamy MK, McKinney EC, Meagher RB. 2005. The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell 17:102633–46
    [Google Scholar]
  29. 29.
    Deal RB, Topp CN, McKinney EC, Meagher RB. 2007. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. .Z. Plant Cell 19:174–83
    [Google Scholar]
  30. 30.
    Dobersch S, Rubio K, Singh I, Günther S, Graumann J et al. 2021. Positioning of nucleosomes containing γ-H2AX precedes active DNA demethylation and transcription initiation. Nat. Commun. 12:11072
    [Google Scholar]
  31. 31.
    Dorigo B, Schalch T, Bystricky K, Richmond TJ. 2003. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327:185–96
    [Google Scholar]
  32. 32.
    Dryhurst D, Ishibashi T, Rose KL, Eirín-López JM, McDonald D et al. 2009. Characterization of the histone H2A.Z-1 and H2A.Z-2 isoforms in vertebrates. BMC Biol. 7:186
    [Google Scholar]
  33. 33.
    Du Y-C, Gu S, Zhou J, Wang T, Cai H et al. 2006. The dynamic alterations of H2AX complex during DNA repair detected by a proteomic approach reveal the critical roles of Ca2+/calmodulin in the ionizing radiation-induced cell cycle arrest. Mol. Cell. Proteom. 5:61033–44
    [Google Scholar]
  34. 34.
    Duc C, Benoit M, Détourné G, Simon L, Poulet A et al. 2017. Arabidopsis ATRX modulates H3.3 occupancy and fine-tunes gene expression. Plant Cell 29:71773–93
    [Google Scholar]
  35. 35.
    Dunn CJ, Sarkar P, Bailey ER, Farris S, Zhao M et al. 2017. Histone hypervariants H2A.Z.1 and H2A.Z.2 play independent and context-specific roles in neuronal activity-induced transcription of Arc/Arg3.1 and other immediate early genes. eNeuro 44ENEURO.0040–17.2017
    [Google Scholar]
  36. 36.
    Eleuteri B, Aranda S, Ernfors P. 2018. NoRC recruitment by H2A.X deposition at rRNA gene promoter limits embryonic stem cell proliferation. Cell Rep. 23:61853–66
    [Google Scholar]
  37. 37.
    Faast R, Thonglairoam V, Schulz TC, Beall J, Wells JRE et al. 2001. Histone variant H2A.Z is required for early mammalian development. Curr. Biol. 11:151183–87
    [Google Scholar]
  38. 38.
    Fan JY, Rangasamy D, Luger K, Tremethick DJ. 2004. H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol. Cell 16:4655–61
    [Google Scholar]
  39. 39.
    Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R et al. 2005. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123:71199–212
    [Google Scholar]
  40. 40.
    Foroozani M, Zahraeifard S, Oh D-H, Wang G, Dassanayake M, Smith AP 2020. Low-phosphate chromatin dynamics predict a cell wall remodeling network in rice shoots. Plant Physiol. 182:31494–509
    [Google Scholar]
  41. 41.
    Gehre M, Bunina D, Sidoli S, Lübke MJ, Diaz N et al. 2020. Lysine 4 of histone H3.3 is required for embryonic stem cell differentiation, histone enrichment at regulatory regions and transcription accuracy. Nat. Genet. 52:3273–82
    [Google Scholar]
  42. 42.
    Gómez-Zambrano Á, Crevillén P, Franco-Zorrilla JM, López JA, Moreno-Romero J et al. 2018. Arabidopsis SWC4 binds DNA and recruits the SWR1 complex to modulate histone H2A.Z deposition at key regulatory genes. Mol. Plant 11:6815–32
    [Google Scholar]
  43. 43.
    Gómez-Zambrano Á, Merini W, Calonje M 2019. The repressive role of Arabidopsis H2A.Z in transcriptional regulation depends on AtBMI1 activity. Nat. Commun. 10:12828
    [Google Scholar]
  44. 44.
    Grasser KD. 2020. The FACT histone chaperone: tuning gene transcription in the chromatin context to modulate plant growth and development. Front. Plant Sci. 11:85
    [Google Scholar]
  45. 45.
    He S, Vickers M, Zhang J, Feng X. 2019. Natural depletion of histone H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation. eLife 8:e42530
    [Google Scholar]
  46. 46.
    Heo K, Kim H, Choi SH, Choi J, Kim K et al. 2008. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 30:186–97
    [Google Scholar]
  47. 47.
    Hetzel J, Duttke SH, Benner C, Chory J. 2016. Nascent RNA sequencing reveals distinct features in plant transcription. PNAS 113:4312316–21Global run-on sequencing reveals a lack of bidirectional transcription in plants.
    [Google Scholar]
  48. 48.
    Hofmann NR. 2016. Last exit to differentiation: histone variants as signposts. Plant Cell 28:61235
    [Google Scholar]
  49. 49.
    Hu G, Cui K, Northrup D, Liu C, Wang C et al. 2013. H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 12:2180–92
    [Google Scholar]
  50. 50.
    Hu Y, Lai Y. 2015. Identification and expression analysis of rice histone genes. Plant Physiol. Biochem. 86:55–65
    [Google Scholar]
  51. 51.
    Huefner ND, Friesner JD, Britt AB. 2009. Characterization of two H2AX homologues in Arabidopsis thaliana and their response to ionizing radiation. Induced Plant Mutations in the GenomicsEra QY Shu 113–17 Rome: Food Agric. Organ. U. N.
    [Google Scholar]
  52. 52.
    Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L et al. 2010. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29:81446–57
    [Google Scholar]
  53. 53.
    Ingouff M, Rademacher S, Holec S, Šoljić L, Xin N et al. 2010. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20:232137–43
    [Google Scholar]
  54. 54.
    Iwasaki YW, Murano K, Ishizu H, Shibuya A, Iyoda Y et al. 2016. Piwi modulates chromatin accessibility by regulating multiple factors including histone H1 to repress transposons. Mol. Cell 63:3408–19
    [Google Scholar]
  55. 55.
    Jacob Y, Bergamin E, Donoghue MTA, Mongeon V, LeBlanc C et al. 2014. Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343:61761249–53
    [Google Scholar]
  56. 56.
    Jarillo JA, Piñeiro M. 2015. H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J. 83:196–109
    [Google Scholar]
  57. 57.
    Jedrusik MA, Schulze E. 2001. A single histone H1 isoform (H1.1) is essential for chromatin silencing and germline development in Caenorhabditis elegans. Development 128:71069–80
    [Google Scholar]
  58. 58.
    Jerzmanowski A, Przewłoka M, Grasser KD. 2000. Linker histones and HMG1 proteins of higher plants. Plant Biol. 2:06586–97
    [Google Scholar]
  59. 59.
    Kasinsky HE, Lewis JD, Dacks JB, Ausló J. 2001. Origin of H1 linker histones. FASEB J. 15:134–42
    [Google Scholar]
  60. 60.
    Kawashima T, Lorković ZJ, Nishihama R, Ishizaki K, Axelsson E et al. 2015. Diversification of histone H2A variants during plant evolution. Trends Plant Sci. 20:7419–25
    [Google Scholar]
  61. 61.
    Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL et al. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A. .Z into euchromatin. PLOS Biol. 2:5e131
    [Google Scholar]
  62. 62.
    Kotliński M, Knizewski L, Muszewska A, Rutowicz K, Lirski M et al. 2017. Phylogeny-based systematization of Arabidopsis proteins with histone H1 globular domain. Plant Physiol. 174:127–34
    [Google Scholar]
  63. 63.
    Kotliński M, Rutowicz K, Kniżewski Ł, Palusiński A, Olędzki J et al. 2016. Histone H1 variants in Arabidopsis are subject to numerous post-translational modifications, both conserved and previously unknown in histones, suggesting complex functions of H1 in plants. PLOS ONE 11:1e0147908
    [Google Scholar]
  64. 64.
    Kralemann LEM, Liu S, Trejo-Arellano MS, Muñoz-Viana R, Köhler C, Hennig L 2020. Removal of H2Aub1 by ubiquitin-specific proteases 12 and 13 is required for stable Polycomb-mediated gene repression in Arabidopsis. Genome Biol. 21:1144
    [Google Scholar]
  65. 65.
    Kumar SV, Wigge PA 2010. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:1136–47
    [Google Scholar]
  66. 66.
    Lang J, Smetana O, Sanchez-Calderon L, Lincker F, Genestier J et al. 2012. Plant γH2AX foci are required for proper DNA DSB repair responses and colocalize with E2F factors. New Phytol. 194:2353–63
    [Google Scholar]
  67. 67.
    Lázaro A, Gómez-Zambrano Á, López-González L, Piñeiro M, Jarillo JA 2008. Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development. J. Exp. Bot. 59:3653–66
    [Google Scholar]
  68. 68.
    Lei B, Berger F. 2020. H2A variants in Arabidopsis: versatile regulators of genome activity. Plant Commun. 1:1100015
    [Google Scholar]
  69. 69.
    Lewis PW, Elsaesser SJ, Noh K-M, Stadler SC, Allis CD. 2010. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. PNAS 107:3214075–80
    [Google Scholar]
  70. 70.
    Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC et al. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:3523–36
    [Google Scholar]
  71. 71.
    Liu C, Cheng Y-J, Wang J-W, Weigel D. 2017. Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat. Plants 3:9742–48
    [Google Scholar]
  72. 72.
    Liu S, de Jonge J, Trejo-Arellano MS, Santos-González J, Köhler C, Hennig L 2021. Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress. New Phytol. 229:42238–50
    [Google Scholar]
  73. 73.
    Liu X, Li B, Gorovsky MA. 1996. Essential and nonessential histone H2A variants in Tetrahymena thermophila. Mol. Cell. Biol. 16:84305–11
    [Google Scholar]
  74. 74.
    Lorković ZJ, Park C, Goiser M, Jiang D, Kurzbauer M-T et al. 2017. Compartmentalization of DNA damage response between heterochromatin and euchromatin is mediated by distinct H2A histone variants. Curr. Biol. 27:81192–99
    [Google Scholar]
  75. 75.
    Lu L, Chen X, Qian S, Zhong X 2018. The plant-specific histone residue Phe41 is important for genome-wide H3.1 distribution. Nat. Commun. 9:1630
    [Google Scholar]
  76. 76.
    Lu X, Wontakal SN, Emelyanov AV, Morcillo P, Konev AY et al. 2009. Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev. 23:4452–65
    [Google Scholar]
  77. 77.
    Lu X, Wontakal SN, Kavi H, Kim BJ, Guzzardo PM et al. 2013. Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3-9. Science 340:612878–81
    [Google Scholar]
  78. 78.
    Luo Y-X, Hou X-M, Zhang C-J, Tan L-M, Shao C-R et al. 2020. A plant-specific SWR1 chromatin-remodeling complex couples histone H2A.Z deposition with nucleosome sliding. EMBO J. 39:7e102008
    [Google Scholar]
  79. 79.
    Malik HS, Henikoff S. 2003. Phylogenomics of the nucleosome. Nat. Struct. Biol. 10:11882–91
    [Google Scholar]
  80. 80.
    Mao Z, Wei X, Li L, Xu P, Zhang J et al. 2021. Arabidopsis cryptochrome 1 controls photomorphogenesis through regulation of H2A.Z deposition. Plant Cell 33:61961–79
    [Google Scholar]
  81. 81.
    March-Díaz R, García-Domínguez M, Lozano-Juste J, León J, Florencio FJ, Reyes JC 2008. Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J. 53:3475–87
    [Google Scholar]
  82. 82.
    March-Díaz R, Reyes JC. 2009. The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol. Plant 2:4565–77
    [Google Scholar]
  83. 83.
    Marques M, Laflamme L, Gervais AL, Gaudreau L. 2010. Reconciling the positive and negative roles of histone H2A.Z in gene transcription. Epigenetics 5:4267–72
    [Google Scholar]
  84. 84.
    Martin-Trillo M, Lázaro A, Poethig RS, Gómez-Mena C, Piñeiro MA et al. 2006. EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development 133:71241–52
    [Google Scholar]
  85. 85.
    Mizuguchi G, Shen X, Landry J, Wu W-H, Sen S, Wu C 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:5656343–48
    [Google Scholar]
  86. 86.
    Molitor AM, Bu Z, Yu Y, Shen WH 2014. Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLOS Genet 10:1e1004091
    [Google Scholar]
  87. 87.
    Moraes I, Yuan Z-F, Liu S, Souza GM, Garcia BA, Casas-Mollano JA. 2015. Analysis of histones H3 and H4 reveals novel and conserved post-translational modifications in sugarcane. PLOS ONE 10:7e0134586
    [Google Scholar]
  88. 88.
    Murphy KE, Meng FW, Makowski CE, Murphy PJ. 2020. Genome-wide chromatin accessibility is restricted by ANP32E. Nat. Commun. 11:15063
    [Google Scholar]
  89. 89.
    Muto S, Senda M, Akai Y, Sato L, Suzuki T et al. 2007. Relationship between the structure of SET/TAF-Iβ/INHAT and its histone chaperone activity. PNAS 104:114285–90
    [Google Scholar]
  90. 90.
    Mylonas C, Lee C, Auld AL, Cisse II, Boyer LA 2021. A dual role for H2A.Z.1 in modulating the dynamics of RNA polymerase II initiation and elongation. Nat. Struct. Mol. Biol. 28:5435–42
    [Google Scholar]
  91. 91.
    Nguyen NH, Cheong J-J. 2018. H2A.Z-containing nucleosomes are evicted to activate AtMYB44 transcription in response to salt stress. Biochem. Biophys. Res. Commun. 499:41039–43
    [Google Scholar]
  92. 92.
    Ni K, Ren J, Xu X, He Y, Finney R et al. 2020. LSH mediates gene repression through macroH2A deposition. Nat. Commun. 11:15647
    [Google Scholar]
  93. 93.
    Nie W-F, Lei M, Zhang M, Tang K, Huang H et al. 2019. Histone acetylation recruits the SWR1 complex to regulate active DNA demethylation in Arabidopsis. PNAS 116:3316641–50
    [Google Scholar]
  94. 94.
    Nie X, Wang H, Li J, Holec S, Berger F 2014. The HIRA complex that deposits the histone H3.3 is conserved in Arabidopsis and facilitates transcriptional dynamics. Biol. Open. 3:9794–802
    [Google Scholar]
  95. 95.
    Nishibuchi I, Suzuki H, Kinomura A, Sun J, Liu N-A et al. 2014. Reorganization of damaged chromatin by the exchange of histone variant H2A.Z-2. Int. J. Radiat. Oncol. Biol. Phys. 89:4736–44
    [Google Scholar]
  96. 96.
    Noh Y-S, Amasino RM. 2003. PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15:71671–82
    [Google Scholar]
  97. 97.
    Okada T, Endo M, Singh MB, Bhalla PL. 2005. Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J. 44:4557–68
    [Google Scholar]
  98. 98.
    Osakabe A, Jamge B, Axelsson E, Montgomery SA, Akimcheva S et al. 2021. The chromatin remodeler DDM1 prevents transposon mobility through deposition of histone variant H2A.W. Nat. Cell Biol. 23:4391–400DDM1 is a depositor of H2A.W, and ddm1 mutants cause derepression of pericentromeric TEs.
    [Google Scholar]
  99. 99.
    Otero S, Desvoyes B, Peiró R, Gutierrez C 2016. Histone H3 dynamics reveal domains with distinct proliferation potential in the Arabidopsis root. Plant Cell 28:61361–71
    [Google Scholar]
  100. 100.
    Park Y-J, Luger K. 2006. The structure of nucleosome assembly protein 1. PNAS 103:51248–53
    [Google Scholar]
  101. 101.
    Patterton HG, Landel CC, Landsman D, Peterson CL, Simpson RT. 1998. The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J. Biol. Chem. 273:137268–76
    [Google Scholar]
  102. 102.
    Paul S. 2021. Histone “acidic patch”: a hotspot in chromatin biology. Nucleus 64:271–75
    [Google Scholar]
  103. 103.
    Piquet S, Le Parc F, Bai S-K, Chevallier O, Adam S, Polo SE 2018. The histone chaperone FACT coordinates H2A.X-dependent signaling and repair of DNA damage. Mol. Cell 72:5888–901.e7
    [Google Scholar]
  104. 104.
    Potok ME, Wang Y, Xu L, Zhong Z, Liu W et al. 2019. Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A. .Z deposition. Nat. Commun. 10:13352
    [Google Scholar]
  105. 105.
    Probst AV, Desvoyes B, Gutierrez C. 2020. Similar yet critically different: the distribution, dynamics and function of histone variants. J. Exp. Bot. 71:175191–204
    [Google Scholar]
  106. 106.
    Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL et al. 2005. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123:2233–48
    [Google Scholar]
  107. 107.
    Rea M, Zheng W, Chen M, Braud C, Bhangu D et al. 2012. Histone H1 affects gene imprinting and DNA methylation in Arabidopsis. Plant J. 71:5776–86
    [Google Scholar]
  108. 108.
    Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM 2011. Recent developments in the use of γ-H2AX as a quantitative DNA double-strand break biomarker. Aging 3:2168–74
    [Google Scholar]
  109. 109.
    Ricketts MD, Frederick B, Hoff H, Tang Y, Schultz DC et al. 2015. Ubinuclein-1 confers histone H3.3-specific-binding by the HIRA histone chaperone complex. Nat. Commun. 6:17711
    [Google Scholar]
  110. 110.
    Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M et al. 2015. Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and Rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol. Cell. Proteom. 14:3556–71
    [Google Scholar]
  111. 111.
    Rosa M, Von Harder M, Cigliano RA, Schlögelhofer P, Mittelsten Scheid O. 2013. The Arabidopsis SWR1 chromatin-remodeling complex is important for DNA repair, somatic recombination, and meiosis. Plant Cell 25:61990–2001
    [Google Scholar]
  112. 112.
    Rutowicz K, Lirski M, Mermaz B, Teano G, Schubert J et al. 2019. Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis. Genome Biol. 20:1157h1 mutants have chromocenter decondensation with minimal transposable element derepression.
    [Google Scholar]
  113. 113.
    Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kotliński M et al. 2015. A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis. Plant Physiol. 169:32080–101
    [Google Scholar]
  114. 114.
    Seo J, Kim SC, Lee H-S, Kim JK, Shon HJ et al. 2012. Genome-wide profiles of H2AX and γ-H2AX differentiate endogenous and exogenous DNA damage hotspots in human cells. Nucleic Acids Res. 40:135965–74
    [Google Scholar]
  115. 115.
    She W, Baroux C. 2015. Chromatin dynamics in pollen mother cells underpin a common scenario at the somatic-to-reproductive fate transition of both the male and female lineages in Arabidopsis. Front. Plant Sci. 6:294
    [Google Scholar]
  116. 116.
    She W, Grimanelli D, Rutowicz K, Whitehead MWJ, Puzio M et al. 2013. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140:194008–19
    [Google Scholar]
  117. 117.
    Shechter D, Chitta RK, Xiao A, Shabanowitz J, Hunt DF, Allis CD. 2009. A distinct H2A.X isoform is enriched in Xenopus laevis eggs and early embryos and is phosphorylated in the absence of a checkpoint. PNAS 106:3749–54
    [Google Scholar]
  118. 118.
    Shen X, Yu L, Weir JW, Gorovsky MA 1995. Linker histories are not essential and affect chromatin condensation in vivo. Cell 82:147–56
    [Google Scholar]
  119. 119.
    Shi L, Wang J, Hong F, Spector DL, Fang Y. 2011. Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. PNAS 108:2610574–78
    [Google Scholar]
  120. 120.
    Shu H, Nakamura M, Siretskiy A, Borghi L, Moraes I et al. 2014. Arabidopsis replacement histone variant H3.3 occupies promoters of regulated genes. Genome Biol. 15:4R62
    [Google Scholar]
  121. 121.
    Sijacic P, Holder DH, Bajic M, Deal RB. 2019. Methyl-CpG-binding domain 9 (MBD9) is required for H2A.Z incorporation into chromatin at a subset of H2A.Z-enriched regions in the Arabidopsis genome. PLOS Genet. 15:8e1008326TAP–Tag protein interaction assay provides new insights into the composition of the plant SWR1 complex.
    [Google Scholar]
  122. 122.
    Singh I, Ozturk N, Cordero J, Mehta A, Hasan D et al. 2015. High mobility group protein-mediated transcription requires DNA damage marker γ-H2AX. Cell Res. 25:7837–50
    [Google Scholar]
  123. 123.
    Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD et al. 2010. Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol. 152:1217–25
    [Google Scholar]
  124. 124.
    Stroud H, Otero S, Desvoyes B, Ramírez-Parra E, Jacobsen SE, Gutierrez C. 2012. Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. PNAS 109:145370–75
    [Google Scholar]
  125. 125.
    Sura W, Kabza M, Karlowski WM, Bieluszewski T, Kus-Slowinska M et al. 2017. Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 29:4791–807
    [Google Scholar]
  126. 126.
    Suto RK, Clarkson MJ, Tremethick DJ, Luger K. 2000. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat. Struct. Biol. 7:121121–24
    [Google Scholar]
  127. 127.
    Talbert PB, Ahmad K, Almouzni G, Ausió J, Berger F et al. 2012. A unified phylogeny-based nomenclature for histone variants. Epigenet. Chromatin 5:7Unified nomenclature for histone variants based on phylogeny as well as historical usage.
    [Google Scholar]
  128. 128.
    Talbert PB, Henikoff S. 2010. Histone variants—ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11:4264–75
    [Google Scholar]
  129. 129.
    Tasset C, Singh Yadav A, Sureshkumar S, Singh R, van der Woude L et al. 2018. POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana. PLOS Genet. 14:3e1007280
    [Google Scholar]
  130. 130.
    Tong M, Lee K, Ezer D, Cortijo S, Jung J et al. 2020. The evening complex establishes repressive chromatin domains via H2A.Z deposition. Plant Physiol. 182:1612–25
    [Google Scholar]
  131. 131.
    Trinklein ND, Aldred SF, Hartman SJ, Schroeder DI, Otillar RP, Myers RM. 2004. An abundance of bidirectional promoters in the human genome. Genome Res. 14:162–66
    [Google Scholar]
  132. 132.
    Ushinsky SC, Bussey H, Ahmed AA, Wang Y, Friesen J et al. 1997. Histone H1 in Saccharomyces cerevisiae. Yeast 13:2151–61
    [Google Scholar]
  133. 133.
    Van Daal A, Elgin SCR. 1992. A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol. Biol. Cell 3:6593–602
    [Google Scholar]
  134. 134.
    Verbsky ML, Richards EJ. 2001. Chromatin remodeling in plants. Curr. Opin. Plant Biol. 4:6494–500
    [Google Scholar]
  135. 135.
    Wang Y, Zhong Z, Zhang Y, Xu L, Feng S et al. 2020. NAP1-RELATED PROTEIN1 and 2 negatively regulate H2A.Z abundance in chromatin in Arabidopsis. Nat. Commun. 11:12887
    [Google Scholar]
  136. 136.
    Waterborg JH. 2012. Evolution of histone H3: emergence of variants and conservation of post-translational modification sites. Biochem. Cell Biol. 90:179–95
    [Google Scholar]
  137. 137.
    Waterborg JH, Robertson AJ. 1996. Common features of analogous replacement histone H3 genes in animals and plants. J. Mol. Evol. 43:3194–206
    [Google Scholar]
  138. 138.
    Waterworth WM, Wilson M, Wang D, Nuhse T, Warward S et al. 2019. Phosphoproteomic analysis reveals plant DNA damage signalling pathways with a functional role for histone H2AX phosphorylation in plant growth under genotoxic stress. Plant J. 100:51007–21
    [Google Scholar]
  139. 139.
    Weber CM, Ramachandran S, Henikoff S. 2014. Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol. Cell 53:5819–30
    [Google Scholar]
  140. 140.
    Willige BC, Zander M, Yoo CY, Phan A, Garza RM et al. 2021. PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants. Nat. Genet. 53:955–61
    [Google Scholar]
  141. 141.
    Wollmann H, Holec S, Alden K, Clarke ND, Jacques P-É, Berger F 2012. Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLOS Genet. 8:5e1002658
    [Google Scholar]
  142. 142.
    Wollmann H, Stroud H, Yelagandula R, Tarutani Y, Jiang D et al. 2017. The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana. Genome Biol. 18:194
    [Google Scholar]
  143. 143.
    Xiao S, Jiang L, Wang C, Ow DW 2021. Arabidopsis OXS3 family proteins repress ABA signaling through interactions with AFP1 in the regulation of ABI4 expression. J. Exp. Bot. 72:155721–34Evidence that phosphorylated H2A.X is required for transcriptional activation—a first for plant biology.
    [Google Scholar]
  144. 144.
    Xu M, Leichty AR, Hu T, Poethig RS. 2018. H2A.Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3. Development 145:2dev152868
    [Google Scholar]
  145. 145.
    Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD. 2012. Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol. Cell 48:5723–33
    [Google Scholar]
  146. 146.
    Xue M, Zhang H, Zhao F, Zhao T, Li H, Jiang D 2021. The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis. Mol. Plant 14:111799–813
    [Google Scholar]
  147. 147.
    Yelagandula R, Stroud H, Holec S, Zhou K, Feng S et al. 2014. The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158:198–109
    [Google Scholar]
  148. 148.
    Zahraeifard S, Foroozani M, Sepehri A, Oh D-H, Wang G et al. 2018. Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes. J. Exp. Bot. 69:204907–19
    [Google Scholar]
  149. 149.
    Zambrano-Mila MS, Aldaz-Villao MJ, Casas-Mollano JA. 2019. Canonical histones and their variants in plants: evolution and functions. Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications R Alvarez-Venegas, C De-la-Peña, J Casas-Mollano 185–222 Cham, Switz.: Springer
    [Google Scholar]
  150. 150.
    Zemach A, Kim MY, Hsieh P-H, Coleman-Derr D, Eshed-Williams L et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:1193–205
    [Google Scholar]
  151. 151.
    Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:61189–201
    [Google Scholar]
  152. 152.
    Zhao F, Zhang H, Zhao T, Li Z, Jiang D 2021. The histone variant H3.3 promotes the active chromatin state to repress flowering in Arabidopsis. Plant Physiol. 186:2051–63H3.3 promotes transcriptional activation of FLC through the formation of a gene loop.
    [Google Scholar]
  153. 153.
    Zhao L, Cai H, Su Z, Wang L, Huang X et al. 2018. KLU suppresses megasporocyte cell fate through SWR1-mediated activation of WRKY28 expression in Arabidopsis. PNAS 115:3E526–35
    [Google Scholar]
  154. 154.
    Zhou B-R, Feng H, Kato H, Dai L, Yang Y et al. 2013. Structural insights into the histone H1-nucleosome complex. PNAS 110:4819390–95
    [Google Scholar]
  155. 155.
    Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S. 2008. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:7218125–29
    [Google Scholar]
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