Advances in Histone Variants in Plant Epigenetic Regulation

doi:10.13560/j.cnki.biotech.bull.1985.2022-0071

Abstract

Abstract:

The basic subunit of chromatin is nucleosome that consists of DNA and histone proteins,and it serves as a carrier of genetic and epigenetic information in regulating life activities. Histone variants are related isoforms in the same histone family. In addition to their sequence divergence,their chromatin assembly is done under specific molecular chaperones. The incorporation of histone variants into nucleosomes generates profound impacts on nucleosome property and chromatin activity. Growing studies in plants support a pivotal role of histone variants in chromatin regulation including chromatin structure and maintenance of the epigenetic information,DNA damage repair and transcription regulation,which subsequently impact plant development and environmental response. Here we summarize recent progress on the chromatin locations of plant histone variants,molecular chaperons and their biological functions,and we propose a few new directions for the study of plant histone variants,aiming to provide a reference for deeply studying the histone variant-mediated epigenetic regulation.

Key words: histone variants, plant, epigenetics, chromatin regulation

XUE Man-de, ZHAO Feng-yue, LI Jie, JIANG Dan-hua. Advances in Histone Variants in Plant Epigenetic Regulation[J]. Biotechnology Bulletin, 2022, 38(7): 1-12.

Figures/Tables 2

Fig. 1 Chromosome and genic distributions of histone variants in A. thaliana

Fig. 2 Role of H2A.Z in photomorphogenesis,shade avo-idance and thermomorphogenesis of A. thaliana Under light conditions,the SWR1 complex interacts with transcription factors and photoreceptors,and deposits H2A.Z at auxin and cell elongation-related genes to repress their expression,resulting in photomorphogenesis. Under low R：FR light or high ambient temperature condition,the INO80 complex interacts with PIF proteins and mediates H2A.Z eviction and transcription activation at their targets,leading to shade avoidance response or thermomorphogenesis respectively

References 108

[1]	Borg M, Jiang DH, Berger F. Histone variants take center stage in shaping the epigenome[J]. Curr Opin Plant Biol, 2021, 61:101991. doi: 10.1016/j.pbi.2020.101991 URL
[2]	Jiang DH, Berger F. Histone variants in plant transcriptional regulation[J]. Biochim Biophys Acta Gene Regul Mech, 2017, 1860(1):123-130. doi: 10.1016/j.bbagrm.2016.07.002 URL
[3]	Kawashima T, Lorković ZJ, Nishihama R, et al. Diversification of histone H2A variants during plant evolution[J]. Trends Plant Sci, 2015, 20(7):419-425. doi: 10.1016/j.tplants.2015.04.005 pmid: 25983206
[4]	Coleman-Derr D, Zilberman D. Deposition of histone variant H2A. Z within gene bodies regulates responsive genes[J]. PLoS Genet, 2012, 8(10):e1002988.
[5]	Dai XZ, Bai YH, Zhao LH, et al. H2A. Z represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in Arabidopsis[J]. Mol Plant, 2017, 10(10):1274-1292. doi: 10.1016/j.molp.2017.09.007 URL
[6]	Giaimo BD, Ferrante F, Herchenröther A, et al. The histone variant H2A. Z in gene regulation[J]. Epigenetics Chromatin, 2019,(1):37.
[7]	Hu GQ, Cui KR, Northrup D, et al. H2A. Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation[J]. Cell Stem Cell, 2013, 12(2):180-192. doi: 10.1016/j.stem.2012.11.003 URL
[8]	Raisner RM, Hartley PD, Meneghini MD, et al. Histone variant H2A. Z marks the 5' ends of both active and inactive genes in euchromatin[J]. Cell, 2005, 123(2):233-248. pmid: 16239142
[9]	Gómez-Zambrano Á, Merini W, Calonje M. The repressive role of Arabidopsis H2A. Z in transcriptional regulation depends on AtBMI1 activity[J]. Nat Commun, 2019, 10(1):2828. doi: 10.1038/s41467-019-10773-1 pmid: 31249301
[10]	Choi K, Park C, Lee J, et al. Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development[J]. Development, 2007, 134(10):1931-1941. doi: 10.1242/dev.001891 URL
[11]	Gómez-Zambrano Á, Crevillén P, Franco-Zorrilla JM, et al. Arabidopsis SWC4 binds DNA and recruits the SWR1 complex to modulate histone H2A. Z deposition at key regulatory genes[J]. Mol Plant, 2018, 11(6):815-832. doi: S1674-2052(18)30122-9 pmid: 29604400
[12]	Nie WF, Lei MG, Zhang MX, et al. Histone acetylation recruits the SWR1 complex to regulate active DNA demethylation in Arabidopsis[J]. Proc Natl Acad Sci USA, 2019, 116(33):16641-16650. doi: 10.1073/pnas.1906023116 URL
[13]	Sijacic P, Holder DH, Bajic M, et al. Methyl-CpG-binding domain 9(MBD9)is required for H2A. Z incorporation into chromatin at a subset of H2A. Z-enriched regions in the Arabidopsisgenome[J]. PLoS Genet, 2019, 15(8):e1008326.
[14]	Luo YX, Hou XM, Zhang CJ, et al. A plant-specific SWR1 chromatin-remodeling complex couples histone H2A. Z deposition with nucleosome sliding[J]. EMBO J, 2020, 39(7):e102008.
[15]	Papamichos-Chronakis M, Watanabe S, Rando OJ, et al. Global regulation of H2A. Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity[J]. Cell, 2011, 144(2):200-213. doi: 10.1016/j.cell.2010.12.021 pmid: 21241891
[16]	Tramantano M, Sun L, Au C, et al. Constitutive turnover of histone H2A. Z at yeast promoters requires the preinitiation complex[J]. eLife, 2016, 5:e14243.
[17]	Ranjan A, Nguyen VQ, Liu S, et al. Live-cell single particle imaging reveals the role of RNA polymerase II in histone H2A. Z eviction[J]. eLife, 2020, 9:e55667.
[18]	Zhang C, Cao L, Rong L, et al. The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development[J]. Plant J, 2015, 82(4):655-668. doi: 10.1111/tpj.12840 URL
[19]	Wang J, Gao S, Peng X, et al. Roles of the INO80 and SWR1 chromatin remodeling complexes in plants[J]. Int J Mol Sci, 2019, 20(18):4591. doi: 10.3390/ijms20184591 URL
[20]	Xue MD, Zhang HR, Zhao FY, et al. The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A. Z eviction and active transcription in Arabidopsis[J]. Mol Plant, 2021, 14(11):1799-1813. doi: 10.1016/j.molp.2021.07.001 URL
[21]	Yang CW, Yin LF, Xie FM, et al. AtINO80 represses photomorphogenesis by modulating nucleosome density and H2A. Z incorporation in light-related genes[J]. Proc Natl Acad Sci USA, 2020, 117(52):33679-33688. doi: 10.1073/pnas.2001976117 URL
[22]	Wang YF, Zhong ZH, Zhang YX, et al. NAP1-RELATED PROTEIN1 and 2 negatively regulate H2A. Z abundance in chromatin in Arabidopsis[J]. Nat Commun, 2020, 11(1):2887. doi: 10.1038/s41467-020-16691-x URL
[23]	Du KX, Luo Q, Yin LF, et al. OsChz1 acts as a histone chaperone in modulating chromatin organization and genome function in rice[J]. Nat Commun, 2020, 11(1):5717. doi: 10.1038/s41467-020-19586-z URL
[24]	Li C, Liu YH, Shen WH, et al. Chromatin-remodeling factor OsINO80 is involved in regulation of gibberellin biosynthesis and is crucial for rice plant growth and development[J]. J Integr Plant Biol, 2018, 60(2):144-159. doi: 10.1111/jipb.12603 URL
[25]	Mao Z, Pan L, Wang WX, et al. Anp32e, a higher eukaryotic histone chaperone directs preferential recognition for H2A. Z[J]. Cell Res, 2014, 24(4):389-399. doi: 10.1038/cr.2014.30 URL
[26]	Obri A, Ouararhni K, Papin C, et al. ANP32E is a histone chaperone that removes H2A. Z from chromatin[J]. Nature, 2014, 505(7485):648-653. doi: 10.1038/nature12922 URL
[27]	Deal RB, Topp CN, McKinney EC, et al. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. Z[J]. Plant Cell, 2007, 19(1):74-83. doi: 10.1105/tpc.106.048447 URL
[28]	Choi K, Kim J, Hwang HJ, et al. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors[J]. Plant Cell, 2011, 23(1):289-303. doi: 10.1105/tpc.110.075911 URL
[29]	Xu ML, Leichty AR, Hu TQ, et al. H2A. Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3[J]. Development, 2018, 145(2):dev152868.
[30]	Zander M, Willige BC, He YP, et al. Epigenetic silencing of a multifunctional plant stress regulator[J]. eLife, 2019, 8:e47835.
[31]	Cai HY, Zhang M, Chai MN, et al. Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A. Z and H3K4me3[J]. New Phytol, 2019, 221(1):295-308. doi: 10.1111/nph.15306 URL
[32]	Yang XD, Zhang XL, Yang YX, et al. The histone variant Sl_H2A. Z regulates carotenoid biosynthesis and gene expression during tomato fruit ripening[J]. Hortic Res, 2021, 8(1):85. doi: 10.1038/s41438-021-00520-3 URL
[33]	March-Díaz R, García-Domínguez M, Lozano-Juste J, et al. Histone H2A. Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis[J]. Plant J, 2008, 53(3):475-487. pmid: 17988222
[34]	Cai HY, Huang YM, Chen FQ, et al. ERECTA signaling regulates plant immune responses via chromatin-mediated promotion of WRKY33 binding to target genes[J]. New Phytol, 2021, 230(2):737-756. doi: 10.1111/nph.17200 URL
[35]	Sura W, Kabza M, Karlowski WM, et al. Dual role of the histone variant H2A. Z in transcriptional regulation of stress-response genes[J]. Plant Cell, 2017, 29(4):791-807. doi: 10.1105/tpc.16.00573 URL
[36]	Nguyen NH, Cheong JJ. H2A. Z-containing nucleosomes are evicted to activate AtMYB44 transcription in response to salt stress[J]. Biochem Biophys Res Commun, 2018, 499(4):1039-1043. doi: 10.1016/j.bbrc.2018.04.048 URL
[37]	Zhu ZQ, Lin CT. Photomorphogenesis:When blue meets red[J]. Nat Plants, 2016, 2:16019. doi: 10.1038/nplants.2016.19 URL
[38]	Zhang CY, Qian Q, Huang X, et al. NF-YCs modulate histone variant H2A. Z deposition to regulate photomorphogenic growth in Arabidopsis[J]. J Integr Plant Biol, 2021, 63(6):1120-1132. doi: 10.1111/jipb.13109 URL
[39]	Nemhauser J, Chory J. Photomorphogenesis[J]. Arabidopsis Book, 2002, 1:e0054.
[40]	Mao ZL, Wei XX, Li L, et al. Arabidopsis cryptochrome 1 controls photomorphogenesis through regulation of H2A. Z deposition[J]. Plant Cell, 2021, 33(6):1961-1979. doi: 10.1093/plcell/koab091 URL
[41]	Wei XX, Wang WT, Xu P, et al. Phytochrome B interacts with SWC6 and ARP6 to regulate H2A. Z deposition and photomorphogensis in Arabidopsis[J]. J Integr Plant Biol, 2021, 63(6):1133-1146. doi: 10.1111/jipb.13111 URL
[42]	Willige BC, Zander M, Yoo CY, et al. PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants[J]. Nat Genet, 2021, 53(7):955-961. doi: 10.1038/s41588-021-00882-3 pmid: 34140685
[43]	Li X, Liang T, Liu HT. How plants coordinate their development in response to light and temperature signals[J]. Plant Cell, 2022, 34(3):955-966. doi: 10.1093/plcell/koab302 URL
[44]	Kumar SV, Wigge PA. H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis[J]. Cell, 2010, 140(1):136-147. doi: 10.1016/j.cell.2009.11.006 URL
[45]	Shang JY, Lu YJ, Cai XW, et al. COMPASS functions as a module of the INO80 chromatin remodeling complex to mediate histone H3K4 methylation in Arabidopsis[J]. Plant Cell, 2021, 33(10):3250-3271. doi: 10.1093/plcell/koab187 URL
[46]	Zahraeifard S, Foroozani M, Sepehri A, et al. Rice H2A. Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes[J]. J Exp Bot, 2018, 69(20):4907-4919. doi: 10.1093/jxb/ery244 pmid: 29955860
[47]	Boden SA, Kavanová M, Finnegan EJ, et al. Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A. Z-nucleosomes[J]. Genome Biol, 2013, 14(6):R65.
[48]	del Olmo I, Poza-Viejo L, Piñeiro M, et al. High ambient temperature leads to reduced FT expression and delayed flowering in Brassica rapa via a mechanism associated with H2A. Z dynamics[J]. Plant J, 2019, 100(2):343-356. doi: 10.1111/tpj.14446 URL
[49]	杨学东, 田守波, 朱为民, 等. 番茄组蛋白变体H2A. Z基因双突变体的获得及其功能研究[J]. 园艺学报, 2018, 45(6):1081-1088.
	Yang XD, Tian SB, Zhu WM, et al. Tomato double mutant of histone variant gene was obtained and its function research[J]. Acta Hortic Sin, 2018, 45(6):1081-1088.
[50]	Bewersdorf J, Bennett BT, Knight KL. H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy[J]. Proc Natl Acad Sci USA, 2006, 103(48):18137-18142. doi: 10.1073/pnas.0608709103 URL
[51]	Yelagandula R, Stroud H, Holec S, et al. The histone variant H2A. W defines heterochromatin and promotes chromatin condensation in Arabidopsis[J]. Cell, 2014, 158(1):98-109. doi: 10.1016/j.cell.2014.06.006 pmid: 24995981
[52]	Lang J, Smetana O, Sanchez-Calderon L, et al. Plant γH2AX foci are required for proper DNA DSB repair responses and colocalize with E2F factors[J]. New Phytol, 2012, 194(2):353-363. doi: 10.1111/j.1469-8137.2012.04062.x URL
[53]	Piquet S le Parc F, Bai SK, et al. The histone chaperone FACT coordinates H2A. X-dependent signaling and repair of DNA damage[J]. Mol Cell, 2018, 72(5):888-901. e7. doi: 10.1016/j.molcel.2018.09.010 URL
[54]	Bourguet P, Picard CL, Yelagandula R, et al. The histone variant H2A. W and linker histone H1 co-regulate heterochromatin accessibility and DNA methylation[J]. Nat Commun, 2021, 12(1):2683. doi: 10.1038/s41467-021-22993-5 pmid: 33976212
[55]	Osakabe A, Jamge B, Axelsson E, et al. The chromatin remodeler DDM1 prevents transposon mobility through deposition of histone variant H2A. W[J]. Nat Cell Biol, 2021, 23(4):391-400. doi: 10.1038/s41556-021-00658-1 URL
[56]	Lorković ZJ, Park C, Goiser M, et al. Compartmentalization of DNA damage response between heterochromatin and euchromatin is mediated by distinct H2A histone variants[J]. Curr Biol, 2017, 27(8):1192-1199. doi: S0960-9822(17)30271-3 pmid: 28392109
[57]	Dalal Y, Bui M. Down the rabbit hole of centromere assembly and dynamics[J]. Curr Opin Cell Biol, 2010, 22(3):392-402. doi: 10.1016/j.ceb.2010.02.005 URL
[58]	Lermontova I, Schubert V, Fuchs J, et al. Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain[J]. Plant Cell, 2006, 18(10):2443-2451. pmid: 17028205
[59]	Fukagawa T, Earnshaw WC. The centromere:chromatin foundation for the kinetochore machinery[J]. Dev Cell, 2014, 30(5):496-508. doi: 10.1016/j.devcel.2014.08.016 pmid: 25203206
[60]	Lermontova I, Koroleva O, Rutten T, et al. Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation[J]. Plant J, 2011, 68(1):40-50. doi: 10.1111/j.1365-313X.2011.04664.x URL
[61]	Teo CH, Lermontova I, Houben A, et al. De novo generation of plant centromeres at tandem repeats[J]. Chromosoma, 2013, 122(3):233-241. doi: 10.1007/s00412-013-0406-0 URL
[62]	Ravi M, Chan SWL. Haploid plants produced by centromere-mediated genome elimination[J]. Nature, 2010, 464(7288):615-618. doi: 10.1038/nature08842 URL
[63]	Lv J, Yu K, Wei J, et al. Generation of paternal haploids in wheat by genome editing of the centromeric histone CENH3[J]. Nat Biotechnol, 2020, 38(12):1397-1401. doi: 10.1038/s41587-020-0728-4 URL
[64]	Wang N, Gent JI, Dawe RK. Haploid induction by a maize cenh3 null mutant[J]. Sci Adv, 2021, 7(4):eabe2299.
[65]	Karimi-Ashtiyani R, Ishii T, Niessen M, et al. Point mutation impairs centromeric CENH3 loading and induces haploid plants[J]. Proc Natl Acad Sci USA, 2015, 112(36):11211-11216. doi: 10.1073/pnas.1504333112 URL
[66]	Kuppu S, Tan EH, Nguyen H, et al. Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance[J]. PLoS Genet, 2015, 11(9):e1005494.
[67]	Maheshwari S, Tan EH, West A, et al. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids[J]. PLoS Genet, 2015, 11(1):e1004970.
[68]	Talbert PB, Ahmad K, Almouzni G, et al. A unified phylogeny-based nomenclature for histone variants[J]. Epigenetics Chromatin, 2012, 5:7. doi: 10.1186/1756-8935-5-7 pmid: 22650316
[69]	Lu L, Chen XS, Qian SM, et al. The plant-specific histone residue Phe41 is important for genome-wide H3. 1 distribution[J]. Nat Commun, 2018, 9(1):630. doi: 10.1038/s41467-017-02454-8 URL
[70]	Szenker E, Ray-Gallet D, Almouzni G. The double face of the histone variant H3. 3[J]. Cell Res, 2011, 21(3):421-434.
[71]	Tagami H, Ray-Gallet D, Almouzni G, et al. Histone H3. 1 and H3. 3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis[J]. Cell, 2004, 116(1):51-61. doi: 10.1016/S0092-8674(03)01064-X URL
[72]	Ahmad K, Henikoff S. The histone variant H3. 3 marks active chromatin by replication-independent nucleosome assembly[J]. Mol Cell, 2002, 9(6):1191-1200. pmid: 12086617
[73]	Nie X, Wang HF, Li J, et al. The HIRA complex that deposits the histone H3. 3 is conserved in Arabidopsis and facilitates transcriptional dynamics[J]. Biol Open, 2014, 3(9):794-802. doi: 10.1242/bio.20148680 URL
[74]	Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin[J]. Cell, 1999, 96(4):575-585. doi: 10.1016/s0092-8674(00)80661-3 pmid: 10052459
[75]	Duc C, Benoit M, Détourné G, et al. Arabidopsis ATRX modulates H3. 3 occupancy and fine-tunes gene expression[J]. Plant Cell, 2017, 29(7):1773-1793. doi: 10.1105/tpc.16.00877 URL
[76]	Lewis PW, Elsaesser SJ, Noh KM, et al. Daxx is an H3. 3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres[J]. Proc Natl Acad Sci USA, 2010, 107(32):14075-14080. doi: 10.1073/pnas.1008850107 URL
[77]	Wang HF, Jiang DH, Axelsson E, et al. LHP1 interacts with ATRX through plant-specific domains at specific loci targeted by PRC2[J]. Mol Plant, 2018, 11(8):1038-1052. doi: 10.1016/j.molp.2018.05.004 URL
[78]	Stroud H, Otero S, Desvoyes B, et al. Genome-wide analysis of histone H3. 1 and H3. 3 variants in Arabidopsis thaliana[J]. Proc Natl Acad Sci USA, 2012, 109(14):5370-5375. doi: 10.1073/pnas.1203145109 URL
[79]	Wollmann H, Holec S, Alden K, et al. Dynamic deposition of histone variant H3. 3 accompanies developmental remodeling of the Arabidopsis transcriptome[J]. PLoS Genet, 2012, 8(5):e1002658.
[80]	Shu H, Nakamura M, Siretskiy A, et al. Arabidopsis replacement histone variant H3. 3 occupies promoters of regulated genes[J]. Genome Biol, 2014, 15(4):R62. doi: 10.1186/gb-2014-15-4-r62 URL
[81]	Mendiratta S, Gatto A, Almouzni G. Histone supply:Multitiered regulation ensures chromatin dynamics throughout the cell cycle[J]. J Cell Biol, 2019, 218(1):39-54. doi: 10.1083/jcb.201807179 pmid: 30257851
[82]	Reverón-Gómez N, González-Aguilera C, Stewart-Morgan KR, et al. Accurate recycling of parental histones reproduces the histone modification landscape during DNA replication[J]. Mol Cell, 2018, 72(2):239-249. e5. doi: S1097-2765(18)30644-0 pmid: 30146316
[83]	Jacob Y, Feng SH, LeBlanc CA, et al. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing[J]. Nat Struct Mol Biol, 2009, 16(7):763-768. doi: 10.1038/nsmb.1611 URL
[84]	Jacob Y, Bergamin E, Donoghue MTA, et al. Selective methylation of histone H3 variant H3. 1 regulates heterochromatin replication[J]. Science, 2014, 343(6176):1249-1253. doi: 10.1126/science.1248357 URL
[85]	Jiang DH, Berger F. DNA replication-coupled histone modification maintains Polycomb gene silencing in plants[J]. Science, 2017, 357(6356):1146-1149. doi: 10.1126/science.aan4965 URL
[86]	Raynaud C, Sozzani R, Glab N, et al. Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen(PCNA)in Arabidopsis[J]. Plant J, 2006, 47(3):395-407. pmid: 16771839
[87]	Dong J, LeBlanc C, Poulet A, et al. H3. 1K27me1 maintains transcriptional silencing and genome stability by preventing GCN5-mediated histone acetylation[J]. Plant Cell, 2021, 33(4):961-979. doi: 10.1093/plcell/koaa027 URL
[88]	Banaszynski LA, Wen DC, Dewell S, et al. Hira-dependent histone H3. 3 deposition facilitates PRC2 recruitment at developmental loci in ES cells[J]. Cell, 2013, 155(1):107-120. doi: 10.1016/j.cell.2013.08.061 pmid: 24074864
[89]	Sitbon D, Boyarchuk E, Dingli F, et al. Histone variant H3. 3 residue S31 is essential for Xenopus gastrulation regardless of the deposition pathway[J]. Nat Commun, 2020, 11(1):1256. doi: 10.1038/s41467-020-15084-4 pmid: 32152320
[90]	Otero S, Desvoyes B, Peiró R, et al. Histone H3 dynamics reveal domains with distinct proliferation potential in the Arabidopsis root[J]. Plant Cell, 2016, 28(6):1361-1371. doi: 10.1105/tpc.15.01003 URL
[91]	Lee LR, Wengier DL, Bergmann DC. Cell-type-specific transcriptome and histone modification dynamics during cellular reprogramming in the Arabidopsis stomatal lineage[J]. Proc Natl Acad Sci USA, 2019, 116(43):21914-21924. doi: 10.1073/pnas.1911400116 URL
[92]	Wollmann H, Stroud H, Yelagandula R, et al. The histone H3 variant H3. 3 regulates gene body DNA methylation in Arabidopsis thaliana[J]. Genome Biol, 2017, 18(1):94. doi: 10.1186/s13059-017-1221-3 pmid: 28521766
[93]	Zhao FY, Zhang HR, Zhao T, et al. The histone variant H3. 3 promotes the active chromatin state to repress flowering in Arabidopsis[J]. Plant Physiol, 2021, 186(4):2051-2063. doi: 10.1093/plphys/kiab224 URL
[94]	Yan A, Borg M, Berger F, et al. The atypical histone variant H3. 15 promotes callus formation in Arabidopsis thaliana[J]. Development, 2020, 147(11):dev184895.
[95]	Borg M, Jacob Y, Susaki D, et al. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin[J]. Nat Cell Biol, 2020, 22(6):621-629. doi: 10.1038/s41556-020-0515-y URL
[96]	Ingouff M, Rademacher S, Holec S, et al. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis[J]. Curr Biol, 2010, 20(23):2137-2143. doi: 10.1016/j.cub.2010.11.012 URL
[97]	Ingouff M, Hamamura Y, Gourgues M, et al. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants[J]. Curr Biol, 2007, 17(12):1032-1037. doi: 10.1016/j.cub.2007.05.019 URL
[98]	Zhao P, Zhou XM, Shen K, et al. Two-step maternal-to-zygotic transition with two-phase parental genome contributions[J]. Dev Cell, 2019, 49(6):882-893. e5. doi: 10.1016/j.devcel.2019.04.016 URL
[99]	Jiang DH, Borg M, Lorković ZJ, et al. The evolution and functional divergence of the histone H2B family in plants[J]. PLoS Genet, 2020, 16(7):e1008964.
[100]	Khadka J, Pesok A, Grafi G. Plant histone HTB(H2B)variants in regulating chromatin structure and function[J]. Plants(Basel), 2020, 2 9(11):1435.
[101]	Zhou BR, Jiang JS, Feng HQ, et al. Structural mechanisms of nucleosome recognition by linker histones[J]. Mol Cell, 2015, 59(4):628-638. doi: 10.1016/j.molcel.2015.06.025 URL
[102]	Bednar J, Garcia-Saez I, Boopathi R, et al. Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1[J]. Mol Cell, 2017, 66(5):729. doi: S1097-2765(17)30358-1 pmid: 28575663
[103]	Kotliński M, Knizewski L, Muszewska A, et al. Phylogeny-based systematization of Arabidopsis proteins with histone H1 globular domain[J]. Plant Physiol, 2017, 174(1):27-34. doi: 10.1104/pp.16.00214 pmid: 28298478
[104]	Rutowicz K, Puzio M, Halibart-Puzio J, et al. A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis[J]. Plant Physiol, 2015, 169(3):2080-2101. doi: 10.1104/pp.15.00493 pmid: 26351307
[105]	Zemach A, Kim MY, Hsieh PH, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin[J]. Cell, 2013, 153(1):193-205. doi: 10.1016/j.cell.2013.02.033 pmid: 23540698
[106]	Rutowicz K, Lirski M, Mermaz B, et al. Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis[J]. Genome Biol, 2019, 20(1):157. doi: 10.1186/s13059-019-1767-3 pmid: 31391082
[107]	Zhang PX, Li XL, Wang YF, et al. PRMT6 physically associates with nuclear factor Y to regulate photoperiodic flowering in Arabidopsis[J]. aBIOTECH, 2021, 2(4):403-414. doi: 10.1007/s42994-021-00065-y URL
[108]	Zhao T, Zhan ZP, Jiang DH. Histone modifications and their regulatory roles in plant development and environmental memory[J]. J Genet Genomics, 2019, 46(10):467-476.