拟南芥雄配子体染色质特征的多组学研究

  有性生殖是大多数动物与高等植物的繁衍方式，生殖细胞的发育一直以来都是发育生物学的研究热点。在哺乳动物中，生殖细胞往往在胚胎时期就已经开始发育和分化，一直持续到性成熟阶段形成成熟的精子或卵子，在这个发育过程中，生殖细胞经历了染色质重编程过程，所以仅有极少数的表观修饰可以遗传至下一代。与哺乳动物不同，高等植物的生殖细胞是在植株发育到一定阶段由体细胞逐步分化发育而来，同时还受到环境因素的影响。拟南芥中成熟的雄配子体也称为花粉，是包含一个营养细胞核和两个精细胞的复杂结构，由同一个小孢子经过有丝分裂而来，但是在之后的双受精作用中两种细胞有着不同的细胞命运。迄今为止，导致营养细胞和精细胞不同分化方向的原因尚未明确，拟南芥的表观特征是否会遗传至下一代这一问题也研究甚少，主要因为难以获得足够的研究材料，加上植物领域表观遗传实验技术的限制，使得这些科学问题一直无法得到解答。在本课题中，我们在已有的高通量测序技术基础上优化了实验方法，使用少量的细胞进行建库测序，分别获得了拟南芥体细胞，小孢子，营养细胞及精细胞的转录组（RNA_seq）和表观遗传组（ATAC-seq，H3K27me3/H3K4me3/H3K9me2 ChIP-seq）的测序数据，并通过整合多组学数据的分析方法，对拟南芥雄配子体发育过程中的表观遗传特征及重编程过程进行探索。

  通过对本课题测序数据进行分析，我们发现拟南芥的精细胞具有广泛的潜在染色质双价性（Bivalency），这些bivalent结构域是在先前已存在的H3K4me3或H3K27me3 domains上再获得H3K27me3或H3K4me3而建立的，并且这些bivalent结构域的组蛋白修饰信号与基因的mRNA水平呈正相关。在精细胞中， H3K27me3 domain上的H3K27me3水平普遍比在体细胞中的H3K27me3水平低，根据H3K27me3水平的变化，我们定义了714个在精细胞中发生H3K27me3重置的基因（H3K27me3 resetting genes），这些基因参与了拟南芥的发育调控。除此之外，我们还发现精细胞的染色质上有组蛋白变体H3.10的渗入，这种渗入有利于形成精细胞独特的H3K27me3 pattern，但是对精细胞中H3K27me3的重置作用却影响甚微。相比之下，营养细胞中建立了上千个H3K27me3 domains，使得大部分与细胞分裂功能相关的基因处于抑制状态，以保证营养细胞一直处在终末分化的细胞状态直至花粉成熟，而授粉相关基因则具备H3K4me3高度覆盖整个基因区的修饰特征，同时有较高的表达水平。除了组蛋白修饰特征之外，相比于精细胞，营养细胞的染色质更加松散，尤其是在着丝粒附近，同时还伴随大量H3K27me3修饰。

  综上所述，我们建立了高灵敏度的ChIP-seq建库体系，在拟南芥的雄配子体中发现了一系列表观遗传特征及其建立过程，为今后对植物生殖细胞的表观遗传研究提供了科学的理论指导和数据支持。

  Sexual reproduction is the way of producing the offspring for most animals and higher plants. The development of germline cells has always been the focus in the field of developmental biology. In mammals, germline cells start to emerge at the early embryonic stage and eventually develop and differentiatied into mature sperms or eggs during sexual maturity stage. During this development process, germline cells undergo the extensive chromatin reprogramming, so that only few epigenetic modifications could be inherited to the next generation. Different from mammals, germline cells of higher plants are gradually differentiated and developed from somatic cells at a later stage. They are prone to be affected by environmental factors. The mature male gametophyte in Arabidopsis thaliana, also known as the pollen, is a complex structure consisting of one vegetative cell nucleus and two sperm cells, all of which are derived from the same microspore through mitosis. However, these two types of cells have distinct cell fates during the subsequent double fertilizations. To date, the causes of the different fates between vegetative cells and sperm cells remain elusive. Whether epigenetic characteristics could be inherited across generations in Arabidopsis is poorly studies. These scientific questions have not been addressed due to the difficulty in obtaining sufficient materials and the limitated sensitivily of epigenetic techniques in plants. In this study, we optimized the experimental procedures based on the existing high-throughput sequencing methods, and used low-input cells to construct the various sequencing libraries. Finally, we obtained the transcriptomics (RNA_seq) and epigenomics (ATAC-seq, H3K27me3/H3K4me3/H3K9me2 ChIP-seq) sequencing data in somatic cells, microspores, vegetative cells and sperm cells of Arabidopsis, respectively, which helps us explore the epigenetic characteristics and the reprogramming process of the male gametophyte development in Arabidopsis thaliana by intergreted analysis the multiple-omics data.

  By analyzing the sequencing data in this study, we found that Arabidopsis sperm cells are featured by widespread potential chromatin bivalency. These bivalent domains are established by the gain of H3K27me3 or H3K4me3 at previously existing H3K4me3 or H3K27me3 domains, respectively. These bivalent domains are related to distict gene mRNA states. In sperm cells, the H3K27me3 level in the H3K27me3 domain is generally lower than that in somatic cells. According to the change of H3K27me3 levels, we identified 714 genes responsible for the resetting of H3K27me3 in sperm cells, which are involved in the regulation of Arabidopsis development. In addition, we also found that the histone variants H3.10 is incorporated into the sperm chromatin, which facilitates the establishment of the unique H3K27me3 patterns in the sperm chromatin, whilst it has a quite limited effect on H3K27me3 resetting. In contrast, the vegetative cell harbors thousands of specific H3K27me3 domains to inhibit most of the genes that are related to cell divisions, so as to ensure that the vegetative cells remain in the state of differentiation until pollen maturation. Pollination-related genes are highly expressed with H3K4me3 covering the entire gene region. In addition to the histone modification features, the chromatin of vegetative cells is more relaxed than that of sperm cells, especially around the pericentromere, and is accompanied by a large amount of H3K27me3 modification.

  In conclusion, we developed an ultrasensitive ChIP-seq method and identified a series of epigenetic features and their establishment processes in male gametophytes of Arabidopsis thaliana, which provides a theoretical guidance and data support for future epigenetic studies in the plant germline.

[1] WADDINGTON C H. The epigenotype. 1942 [J]. Int J Epidemiol, 2012, 41(1): 10-3.
[2] BIRD A. Perceptions of epigenetics [J]. Nature, 2007, 447(7143): 396-8.
[3] BERGER S L, KOUZARIDES T, SHIEKHATTAR R, et al. An operational definition of epigenetics [J]. Genes Dev, 2009, 23(7): 781-3.
[4] KORNBERG R D, THOMAS J O. Chromatin structure; oligomers of the histones [J]. Science, 1974, 184(4139): 865-8.
[5] KAPLAN N, MOORE I K, FONDUFE-MITTENDORF Y, et al. The DNA-encoded nucleosome organization of a eukaryotic genome [J]. Nature, 2009, 458(7236): 362-6.
[6] KORNBERG R D. Chromatin structure: a repeating unit of histones and DNA [J]. Science, 1974, 184(4139): 868-71.
[7] CRANE-ROBINSON C, HEBBES T R, CLAYTON A L, et al. Chromosomal mapping of core histone acetylation by immunoselection [J]. Methods, 1997, 12(1): 48-56.
[8] PECINKA A, MITTELSTEN SCHEID O. Stress-induced chromatin changes: a critical view on their heritability [J]. Plant Cell Physiol, 2012, 53(5): 801-8.
[9] MCKEOWN P C, SPILLANE C. Landscaping plant epigenetics [J]. Methods Mol Biol, 2014, 1112: 1-24.
[10] JENUWEIN T, ALLIS C D. Translating the histone code [J]. Science, 2001, 293(5532): 1074-80.
[11] XU Q, XIE W. Epigenome in Early Mammalian Development: Inheritance, Reprogramming and Establishment [J]. Trends Cell Biol, 2018, 28(3): 237-53.
[12] ZENG Y, CHEN T. DNA methylation reprogramming during mammalian development [J]. Genes (Basel), 2019, 10(4).
[13] DELAVAL K, FEIL R. Epigenetic regulation of mammalian genomic imprinting [J]. Curr Opin Genet Dev, 2004, 14(2): 188-95.
[14] WANG J W, QI Y. Plant non-coding RNAs and epigenetics [J]. Sci China Life Sci, 2018, 61(2): 135-7.
[15] BAURLE I, DEAN C. The timing of developmental transitions in plants [J]. Cell, 2006, 125(4): 655-64.
[16] TSUCHIYA T, EULGEM T. The Arabidopsis defense component EDM2 affects the floral transition in an FLC-dependent manner [J]. Plant J, 2010, 62(3): 518-28.
[17] KUNDARIYA H, YANG X, MORTON K, et al. MSH1-induced heritable enhanced growth vigor through grafting is associated with the RdDM pathway in plants [J]. Nat Commun, 2020, 11(1): 5343.
[18] CHEN K, ZHAO B S, HE C. Nucleic acid modifications in regulation of gene expression [J]. Cell Chem Biol, 2016, 23(1): 74-85.
[19] ZHANG G, HUANG H, LIU D, et al. N6-methyladenine DNA modification in Drosophila [J]. Cell, 2015, 161(4): 893-906.
[20] FROMMER M, MCDONALD L E, MILLAR D S, et al. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands [J]. Proc Natl Acad Sci U S A, 1992, 89(5): 1827-31.
[21] MELNIKOV A A, GARTENHAUS R B, LEVENSON A S, et al. MSRE-PCR for analysis of gene-specific DNA methylation [J]. Nucleic Acids Res, 2005, 33(10): e93.
[22] SCHADT E E, TURNER S, KASARSKIS A. A window into third-generation sequencing [J]. Hum Mol Genet, 2010, 19(R2): R227-40.
[23] YU M, HON G C, SZULWACH K E, et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome [J]. Cell, 2012, 149(6): 1368-80.
[24] LI B, CAREY M, WORKMAN J L. The role of chromatin during transcription [J]. Cell, 2007, 128(4): 707-19.
[25] CHEN X, MIRAGAIA R J, NATARAJAN K N, et al. A rapid and robust method for single cell chromatin accessibility profiling [J]. Nat Commun, 2018, 9(1): 5345.
[26] KLEMM S L, SHIPONY Z, GREENLEAF W J. Chromatin accessibility and the regulatory epigenome [J]. Nat Rev Genet, 2019, 20(4): 207-20.
[27] ZARET K. Micrococcal nuclease analysis of chromatin structure [J]. Curr Protoc Mol Biol, 2005, Chapter 21: Unit 21 1.
[28] PAJORO A, MUINO J M, ANGENENT G C, et al. Profiling nucleosome occupancy by MNase-seq: experimental protocol and computational analysis [J]. Methods Mol Biol, 2018, 1675: 167-81.
[29] SONG L, CRAWFORD G E. DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells [J]. Cold Spring Harb Protoc, 2010, 2010(2): pdb prot5384.
[30] BUENROSTRO J D, GIRESI P G, ZABA L C, et al. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position [J]. Nat Methods, 2013, 10(12): 1213-8.
[31] LI N, JIN K, BAI Y, et al. Tn5 Transposase Applied in Genomics Research [J]. Int J Mol Sci, 2020, 21(21).
[32] ADEY A, MORRISON H G, ASAN, et al. Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition [J]. Genome Biol, 2010, 11(12): R119.
[33] BAJIC M, MAHER K A, DEAL R B. Identification of open chromatin regions in plant genomes using ATAC-Seq [J]. Methods Mol Biol, 2018, 1675: 183-201.
[34] BANNISTER A J, KOUZARIDES T. Regulation of chromatin by histone modifications [J]. Cell Res, 2011, 21(3): 381-95.
[35] GADE P, KALVAKOLANU D V. Chromatin immunoprecipitation assay as a tool for analyzing transcription factor activity [J]. Methods Mol Biol, 2012, 809: 85-104.
[36] BARSKI A, CUDDAPAH S, CUI K, et al. High-resolution profiling of histone methylations in the human genome [J]. Cell, 2007, 129(4): 823-37.
[37] SCHMID M, DURUSSEL T, LAEMMLI U K. ChIC and ChEC; genomic mapping of chromatin proteins [J]. Mol Cell, 2004, 16(1): 147-57.
[38] SKENE P J, HENIKOFF S. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites [J]. Elife, 2017, 6.
[39] SKENE P J, HENIKOFF J G, HENIKOFF S. Targeted in situ genome-wide profiling with high efficiency for low cell numbers [J]. Nat Protoc, 2018, 13(5): 1006-19.
[40] HAINER S J, BOSKOVIC A, MCCANNELL K N, et al. Profiling of pluripotency factors in single cells and early embryos [J]. Cell, 2019, 177(5): 1319-29 e11.
[41] KAYA-OKUR H S, WU S J, CODOMO C A, et al. CUT&Tag for efficient epigenomic profiling of small samples and single cells [J]. Nat Commun, 2019, 10(1): 1930.
[42] DEKKER J, RIPPE K, DEKKER M, et al. Capturing chromosome conformation [J]. Science, 2002, 295(5558): 1306-11.
[43] ZHAO Z, TAVOOSIDANA G, SJOLINDER M, et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions [J]. Nat Genet, 2006, 38(11): 1341-7.
[44] DOSTIE J, RICHMOND T A, ARNAOUT R A, et al. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements [J]. Genome Res, 2006, 16(10): 1299-309.
[45] HORIKE S, CAI S, MIYANO M, et al. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome [J]. Nat Genet, 2005, 37(1): 31-40.
[46] FULLWOOD M J, LIU M H, PAN Y F, et al. An oestrogen-receptor-alpha-bound human chromatin interactome [J]. Nature, 2009, 462(7269): 58-64.
[47] LIEBERMAN-AIDEN E, VAN BERKUM N L, WILLIAMS L, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome [J]. Science, 2009, 326(5950): 289-93.
[48] DI PIERRO M, CHENG R R, LIEBERMAN AIDEN E, et al. De novo prediction of human chromosome structures: Epigenetic marking patterns encode genome architecture [J]. Proc Natl Acad Sci U S A, 2017, 114(46): 12126-31.
[49] QI Y, ZHANG B. Predicting three-dimensional genome organization with chromatin states [J]. PLoS Comput Biol, 2019, 15(6): e1007024.
[50] WANG Z, GERSTEIN M, SNYDER M. RNA-Seq: a revolutionary tool for transcriptomics [J]. Nat Rev Genet, 2009, 10(1): 57-63.
[51] RAMSKOLD D, LUO S, WANG Y C, et al. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells [J]. Nat Biotechnol, 2012, 30(8): 777-82.
[52] PICELLI S, BJORKLUND A K, FARIDANI O R, et al. Smart-seq2 for sensitive full-length transcriptome profiling in single cells [J]. Nat Methods, 2013, 10(11): 1096-8.
[53] HAGEMANN-JENSEN M, ZIEGENHAIN C, CHEN P, et al. Single-cell RNA counting at allele and isoform resolution using Smart-seq3 [J]. Nat Biotechnol, 2020, 38(6): 708-14.
[54] SAWAN C, HERCEG Z. Histone modifications and cancer [J]. Adv Genet, 2010, 70: 57-85.
[55] MARGUERON R, TROJER P, REINBERG D. The key to development: interpreting the histone code? [J]. Curr Opin Genet Dev, 2005, 15(2): 163-76.
[56] BANERJEE T, CHAKRAVARTI D. A peek into the complex realm of histone phosphorylation [J]. Mol Cell Biol, 2011, 31(24): 4858-73.
[57] KAIMORI J Y, MAEHARA K, HAYASHI-TAKANAKA Y, et al. Histone H4 lysine 20 acetylation is associated with gene repression in human cells [J]. Sci Rep, 2016, 6: 24318.
[58] KHAN S A, REDDY D, GUPTA S. Global histone post-translational modifications and cancer: Biomarkers for diagnosis, prognosis and treatment? [J]. World J Biol Chem, 2015, 6(4): 333-45.
[59] ZHAO S, ALLIS C D, WANG G G. The language of chromatin modification in human cancers [J]. Nat Rev Cancer, 2021, 21(7): 413-30.
[60] RAMAZI S, ALLAHVERDI A, ZAHIRI J. Evaluation of post-translational modifications in histone proteins: A review on histone modification defects in developmental and neurological disorders [J]. J Biosci, 2020, 45.
[61] CARTER B, BISHOP B, HO K K, et al. The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis [J]. Plant Cell, 2018, 30(6): 1337-52.
[62] ARANDA S, MAS G, DI CROCE L. Regulation of gene transcription by Polycomb proteins [J]. Sci Adv, 2015, 1(11): e1500737.
[63] LAUBERTH S M, NAKAYAMA T, WU X, et al. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation [J]. Cell, 2013, 152(5): 1021-36.
[64] LAWRENCE M, DAUJAT S, SCHNEIDER R. Lateral thinking: How histone modifications regulate gene expression [J]. Trends Genet, 2016, 32(1): 42-56.
[65] ZHOU V W, GOREN A, BERNSTEIN B E. Charting histone modifications and the functional organization of mammalian genomes [J]. Nat Rev Genet, 2011, 12(1): 7-18.
[66] CALO E, WYSOCKA J. Modification of enhancer chromatin: what, how, and why? [J]. Mol Cell, 2013, 49(5): 825-37.
[67] BERNSTEIN B E, MIKKELSEN T S, XIE X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells [J]. Cell, 2006, 125(2): 315-26.
[68] AZUARA V, PERRY P, SAUER S, et al. Chromatin signatures of pluripotent cell lines [J]. Nat Cell Biol, 2006, 8(5): 532-8.
[69] PAN G, TIAN S, NIE J, et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells [J]. Cell Stem Cell, 2007, 1(3): 299-312.
[70] ZHAO X D, HAN X, CHEW J L, et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells [J]. Cell Stem Cell, 2007, 1(3): 286-98.
[71] SAXONOV S, BERG P, BRUTLAG D L. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters [J]. Proc Natl Acad Sci U S A, 2006, 103(5): 1412-7.
[72] DEATON A M, BIRD A. CpG islands and the regulation of transcription [J]. Genes Dev, 2011, 25(10): 1010-22.
[73] WEBER M, HELLMANN I, STADLER M B, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome [J]. Nat Genet, 2007, 39(4): 457-66.
[74] MEISSNER A, MIKKELSEN T S, GU H, et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells [J]. Nature, 2008, 454(7205): 766-70.
[75] FOUSE S D, SHEN Y, PELLEGRINI M, et al. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation [J]. Cell Stem Cell, 2008, 2(2): 160-9.
[76] GUENTHER M G, LEVINE S S, BOYER L A, et al. A chromatin landmark and transcription initiation at most promoters in human cells [J]. Cell, 2007, 130(1): 77-88.
[77] MIKKELSEN T S, KU M, JAFFE D B, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells [J]. Nature, 2007, 448(7153): 553-60.
[78] VOIGT P, TEE W W, REINBERG D. A double take on bivalent promoters [J]. Genes Dev, 2013, 27(12): 1318-38.
[79] BAPAT S A, JIN V, BERRY N, et al. Multivalent epigenetic marks confer microenvironment-responsive epigenetic plasticity to ovarian cancer cells [J]. Epigenetics, 2010, 5(8): 716-29.
[80] RODRIGUEZ J, MUNOZ M, VIVES L, et al. Bivalent domains enforce transcriptional memory of DNA methylated genes in cancer cells [J]. Proc Natl Acad Sci U S A, 2008, 105(50): 19809-14.
[81] MCGARVEY K M, VAN NESTE L, COPE L, et al. Defining a chromatin pattern that characterizes DNA-hypermethylated genes in colon cancer cells [J]. Cancer Res, 2008, 68(14): 5753-9.
[82] ALDER O, LAVIAL F, HELNESS A, et al. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment [J]. Development, 2010, 137(15): 2483-92.
[83] DAHL J A, REINER A H, KLUNGLAND A, et al. Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos [J]. PLoS One, 2010, 5(2): e9150.
[84] RUGG-GUNN P J, COX B J, RALSTON A, et al. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo [J]. Proc Natl Acad Sci U S A, 2010, 107(24): 10783-90.
[85] MOHN F, WEBER M, REBHAN M, et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors [J]. Mol Cell, 2008, 30(6): 755-66.
[86] AKKERS R C, VAN HEERINGEN S J, JACOBI U G, et al. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos [J]. Dev Cell, 2009, 17(3): 425-34.
[87] CUI K, ZANG C, ROH T Y, et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation [J]. Cell Stem Cell, 2009, 4(1): 80-93.
[88] MATSUMURA Y, NAKAKI R, INAGAKI T, et al. H3K4/H3K9me3 bivalent chromatin domains targeted by lineage-specific DNA methylation pauses adipocyte differentiation [J]. Mol Cell, 2015, 60(4): 584-96.
[89] XU J, KIDDER B L. H4K20me3 co-localizes with activating histone modifications at transcriptionally dynamic regions in embryonic stem cells [J]. BMC Genomics, 2018, 19(1): 514.
[90] ZENG Z, ZHANG W, MARAND A P, et al. Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato [J]. Genome Biol, 2019, 20(1): 123.
[91] ZHANG Q, GUAN P, ZHAO L, et al. Asymmetric epigenome maps of subgenomes reveal imbalanced transcription and distinct evolutionary trends in Brassica napus [J]. Mol Plant, 2021, 14(4): 604-19.
[92] ZHAO K, KONG D, JIN B, et al. A novel bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis [J]. Elife, 2021, 10.
[93] REIK W, SURANI M A. Germline and pluripotent stem Cells [J]. Cold Spring Harb Perspect Biol, 2015, 7(11).
[94] TANG W W, KOBAYASHI T, IRIE N, et al. Specification and epigenetic programming of the human germ line [J]. Nat Rev Genet, 2016, 17(10): 585-600.
[95] KOTA S K, FEIL R. Epigenetic transitions in germ cell development and meiosis [J]. Dev Cell, 2010, 19(5): 675-86.
[96] GAUCHER J, REYNOIRD N, MONTELLIER E, et al. From meiosis to postmeiotic events: the secrets of histone disappearance [J]. FEBS J, 2010, 277(3): 599-604.
[97] KIMMINS S, SASSONE-CORSI P. Chromatin remodelling and epigenetic features of germ cells [J]. Nature, 2005, 434(7033): 583-9.
[98] BARRAL S, MOROZUMI Y, TANAKA H, et al. Histone variant H2A.L.2 guides transition protein-dependent protamine assembly in male germ cells [J]. Mol Cell, 2017, 66(1): 89-101 e8.
[99] MORITZ L, HAMMOUD S S. The art of packaging the sperm genome: molecular and structural basis of the histone-to-protamine exchange [J]. Front Endocrinol (Lausanne), 2022, 13: 895502.
[100]ITOH K, KONDOH G, MIYACHI H, et al. Dephosphorylation of protamine 2 at serine 56 is crucial for murine sperm maturation in vivo [J]. Sci Signal, 2019, 12(574).
[101]GOU L T, LIM D H, MA W, et al. Initiation of parental genome reprogramming in fertilized oocyte by splicing kinase SRPK1-catalyzed protamine phosphorylation [J]. Cell, 2020, 180(6): 1212-27 e14.
[102]RATHKE C, BAARENDS W M, AWE S, et al. Chromatin dynamics during spermiogenesis [J]. Biochim Biophys Acta, 2014, 1839(3): 155-68.
[103]ANDRES F, COUPLAND G. The genetic basis of flowering responses to seasonal cues [J]. Nat Rev Genet, 2012, 13(9): 627-39.
[104]KINOSHITA A, VAYSSIERES A, RICHTER R, et al. Regulation of shoot meristem shape by photoperiodic signaling and phytohormones during floral induction of Arabidopsis [J]. Elife, 2020, 9.
[105]SCOTT R J, SPIELMAN M, DICKINSON H G. Stamen structure and function [J]. Plant Cell, 2004, 16 Suppl(Suppl): S46-60.
[106]HACKENBERG D, TWELL D. The evolution and patterning of male gametophyte development [J]. Curr Top Dev Biol, 2019, 131: 257-98.
[107]HAFIDH S, FILA J, HONYS D. Male gametophyte development and function in angiosperms: a general concept [J]. Plant Reprod, 2016, 29(1-2): 31-51.
[108]LONG M, SUN X, SHI W, et al. A novel histone H4 variant H4G regulates rDNA transcription in breast cancer [J]. Nucleic Acids Res, 2019, 47(16): 8399-409.
[109]PROBST A V, DESVOYES B, GUTIERREZ C. Similar yet critically different: the distribution, dynamics and function of histone variants [J]. J Exp Bot, 2020, 71(17): 5191-204.
[110]TALBERT P B, AHMAD K, ALMOUZNI G, et al. A unified phylogeny-based nomenclature for histone variants [J]. Epigenetics Chromatin, 2012, 5: 7.
[111]TALBERT P B, HENIKOFF S. Histone variants on the move: substrates for chromatin dynamics [J]. Nat Rev Mol Cell Biol, 2017, 18(2): 115-26.
[112]HENIKOFF S, SMITH M M. Histone variants and epigenetics [J]. Cold Spring Harb Perspect Biol, 2015, 7(1): a019364.
[113]PROBST A V. Deposition and eviction of histone variants define functional chromatin states in plants [J]. Curr Opin Plant Biol, 2022, 69: 102266.
[114]NUNEZ-VAZQUEZ R, DESVOYES B, GUTIERREZ C. Histone variants and modifications during abiotic stress response [J]. Front Plant Sci, 2022, 13: 984702.
[115]ROSA S, SHAW P. Insights into chromatin structure and dynamics in plants [J]. Biology (Basel), 2013, 2(4): 1378-410.
[116]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 U S A, 2012, 109(14): 5370-5.
[117]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.
[118]SEQUEIRA-MENDES J, ARAGUEZ I, PEIRO R, et al. The functional topography of the Arabidopsis genome Is organized in a reduced number of linear motifs of chromatin states [J]. Plant Cell, 2014, 26(6): 2351-66.
[119]BORG M, JIANG D, BERGER F. Histone variants take center stage in shaping the epigenome [J]. Curr Opin Plant Biol, 2021, 61: 101991.
[120]GREWAL S I, JIA S. Heterochromatin revisited [J]. Nat Rev Genet, 2007, 8(1): 35-46.
[121]VAILLANT I, PASZKOWSKI J. Role of histone and DNA methylation in gene regulation [J]. Curr Opin Plant Biol, 2007, 10(5): 528-33.
[122]ROUDIER F, TEIXEIRA F K, COLOT V. Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more [J]. Trends Genet, 2009, 25(11): 511-7.
[123]ZEMACH A, KIM M Y, HSIEH P H, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin [J]. Cell, 2013, 153(1): 193-205.
[124]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.
[125]CHOI J, LYONS D B, KIM M Y, et al. DNA methylation and histone H1 Jointly repress transposable elements and aberrant intragenic transcripts [J]. Mol Cell, 2020, 77(2): 310-23 e7.
[126]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): 2137-43.
[127]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): 621-9.
[128]BUTTRESS T, HE S, WANG L, et al. Histone H2B.8 compacts flowering plant sperm through chromatin phase separation [J]. Nature, 2022, 611(7936): 614-22.
[129]BOURGUET P, PICARD C L, 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.
[130]SHE W, BAROUX C. 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 [J]. Front Plant Sci, 2015, 6: 294.
[131]XIAO S, JIANG L, WANG C, et al. Arabidopsis OXS3 family proteins repress ABA signaling through interactions with AFP1 in the regulation of ABI4 expression [J]. J Exp Bot, 2021, 72(15): 5721-34.
[132]JARILLO J A, PINEIRO M. H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis [J]. Plant J, 2015, 83(1): 96-109.
[133]GOMEZ-ZAMBRANO A, 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.
[134]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): 1931-41.
[135]DEAL R B, TOPP C N, MCKINNEY E C, 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.
[136]MARTIN-TRILLO M, LAZARO A, POETHIG R S, et al. 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 [J]. Development, 2006, 133(7): 1241-52.
[137]NOH Y S, AMASINO R M. PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis [J]. Plant Cell, 2003, 15(7): 1671-82.
[138]SIJACIC P, HOLDER D H, 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 Arabidopsis genome [J]. PLoS Genet, 2019, 15(8): e1008326.
[139]GOMEZ-ZAMBRANO A, CREVILLEN P, FRANCO-ZORRILLA J M, 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): 815-32.
[140]XU M, LEICHTY A R, HU T, et al. H2A.Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3 [J]. Development, 2018, 145(2).
[141]CAI H, ZHANG M, CHAI M, et al. Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3 [J]. New Phytol, 2019, 221(1): 295-308.
[142]ZHAO L, CAI H, SU Z, et al. KLU suppresses megasporocyte cell fate through SWR1-mediated activation of WRKY28 expression in Arabidopsis [J]. Proc Natl Acad Sci U S A, 2018, 115(3): E526-E35.
[143]TONG M, LEE K, EZER D, et al. The evening complex establishes repressive chromatin domains via H2A.Z deposition [J]. Plant Physiol, 2020, 182(1): 612-25.
[144]JIANG D, BORG M, LORKOVIC Z J, et al. The evolution and functional divergence of the histone H2B family in plants [J]. PLoS Genet, 2020, 16(7): e1008964.
[145]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.
[146]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).
[147]XIAO J, LEE U S, WAGNER D. Tug of war: adding and removing histone lysine methylation in Arabidopsis [J]. Curr Opin Plant Biol, 2016, 34: 41-53.
[148]CHENG K, XU Y, YANG C, et al. Histone tales: lysine methylation, a protagonist in Arabidopsis development [J]. J Exp Bot, 2020, 71(3): 793-807.
[149]ZHANG K, SRIDHAR V V, ZHU J, et al. Distinctive core histone post-translational modification patterns in Arabidopsis thaliana [J]. PLoS One, 2007, 2(11): e1210.
[150]PATEL D J. A structural perspective on readout of epigenetic histone and DNA methylation Marks [J]. Cold Spring Harb Perspect Biol, 2016, 8(3): a018754.
[151]HU H, DU J. Structure and mechanism of histone methylation dynamics in Arabidopsis [J]. Curr Opin Plant Biol, 2022, 67: 102211.
[152]NG D W, WANG T, CHANDRASEKHARAN M B, et al. Plant SET domain-containing proteins: structure, function and regulation [J]. Biochim Biophys Acta, 2007, 1769(5-6): 316-29.
[153]ZHOU H, LIU Y, LIANG Y, et al. The function of histone lysine methylation related SET domain group proteins in plants [J]. Protein Sci, 2020, 29(5): 1120-37.
[154]LAFOS M, KROLL P, HOHENSTATT M L, et al. Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation [J]. PLoS Genet, 2011, 7(4): e1002040.
[155]TANG X, LIM M H, PELLETIER J, et al. Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings [J]. J Exp Bot, 2012, 63(3): 1391-404.
[156]JACOB Y, STROUD H, LEBLANC C, et al. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases [J]. Nature, 2010, 466(7309): 987-91.
[157]CARTAGENA J A, MATSUNAGA S, SEKI M, et al. The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen [J]. Dev Biol, 2008, 315(2): 355-68.
[158]GRINI P E, THORSTENSEN T, ALM V, et al. The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis [J]. PLoS One, 2009, 4(11): e7817.
[159]GUO L, YU Y, LAW J A, et al. SET DOMAIN GROUP2 is the major histone H3 lysine [corrected] 4 trimethyltransferase in Arabidopsis [J]. Proc Natl Acad Sci U S A, 2010, 107(43): 18557-62.
[160]ALVAREZ-VENEGAS R, PIEN S, SADDER M, et al. ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes [J]. Curr Biol, 2003, 13(8): 627-37.
[161]KRICHEVSKY A, GUTGARTS H, KOZLOVSKY S V, et al. C2H2 zinc finger-SET histone methyltransferase is a plant-specific chromatin modifier [J]. Dev Biol, 2007, 303(1): 259-69.
[162]LU F, LI G, CUI X, et al. Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice [J]. J Integr Plant Biol, 2008, 50(7): 886-96.
[163]SHI Y, LAN F, MATSON C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1 [J]. Cell, 2004, 119(7): 941-53.
[164]TSUKADA Y, FANG J, ERDJUMENT-BROMAGE H, et al. Histone demethylation by a family of JmjC domain-containing proteins [J]. Nature, 2006, 439(7078): 811-6.
[165]YAMAGUCHI N. Removal of H3K27me3 by JMJ proteins controls plant development and environmental responses in Arabidopsis [J]. Front Plant Sci, 2021, 12: 687416.
[166]KEYZOR C, MERMAZ B, TRIGAZIS E, et al. Histone demethylases ELF6 and JMJ13 antagonistically regulate self-fertility in Arabidopsis [J]. Front Plant Sci, 2021, 12: 640135.
[167]PAN J, ZHANG H, ZHAN Z, et al. A REF6-dependent H3K27me3-depleted state facilitates gene activation during germination in Arabidopsis [J]. J Genet Genomics, 2022.
[168]YANG H, HAN Z, CAO Y, et al. A companion cell-dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression [J]. PLoS Genet, 2012, 8(4): e1002664.
[169]SHEN Y, CONDE E S N, AUDONNET L, et al. Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis [J]. Front Plant Sci, 2014, 5: 290.
[170]CATTANEO P, GRAEFF M, MARHAVA P, et al. Conditional effects of the epigenetic regulator JUMONJI 14 in Arabidopsis root growth [J]. Development, 2019, 146(23).
[171]LIU P, ZHANG S, ZHOU B, et al. The Histone H3K4 demethylase JMJ16 represses leaf senescence in Arabidopsis [J]. Plant Cell, 2019, 31(2): 430-43.
[172]HUANG S, ZHANG A, JIN J B, et al. Arabidopsis histone H3K4 demethylase JMJ17 functions in dehydration stress response [J]. New Phytol, 2019, 223(3): 1372-87.
[173]ISLAM M T, WANG L C, CHEN I J, et al. Arabidopsis JMJ17 promotes cotyledon greening during de-etiolation by repressing genes involved in tetrapyrrole biosynthesis in etiolated seedlings [J]. New Phytol, 2021, 231(3): 1023-39.
[174]AUDONNET L, SHEN Y, ZHOU D X. JMJ24 antagonizes histone H3K9 demethylase IBM1/JMJ25 function and interacts with RNAi pathways for gene silencing [J]. Gene Expr Patterns, 2017, 25-26: 1-7.
[175]FAN D, WANG X, TANG X, et al. Histone H3K9 demethylase JMJ25 epigenetically modulates anthocyanin biosynthesis in poplar [J]. Plant J, 2018, 96(6): 1121-36.
[176]WANG Q, LIU P, JING H, et al. JMJ27-mediated histone H3K9 demethylation positively regulates drought-stress responses in Arabidopsis [J]. New Phytol, 2021, 232(1): 221-36.
[177]CHENG J, XU L, BERGER V, et al. H3K9 demethylases IBM1 and JMJ27 are required for male meiosis in Arabidopsis thaliana [J]. New Phytol, 2022, 235(6): 2252-69.
[178]HUNG F Y, LAI Y C, WANG J, et al. The Arabidopsis histone demethylase JMJ28 regulates CONSTANS by interacting with FBH transcription factors [J]. Plant Cell, 2021, 33(4): 1196-211.
[179]HUNG F Y, CHEN J H, FENG Y R, et al. Arabidopsis JMJ29 is involved in trichome development by regulating the core trichome initiation gene GLABRA3 [J]. Plant J, 2020, 103(5): 1735-43.
[180]LEE H G, SEO P J. The Arabidopsis JMJ29 protein controls circadian oscillation through diurnal histone demethylation at the CCA1 and PRR9 Loci [J]. Genes (Basel), 2021, 12(4).
[181]CHO J N, RYU J Y, JEONG Y M, et al. Control of seed germination by light-induced histone arginine demethylation activity [J]. Dev Cell, 2012, 22(4): 736-48.
[182]BORGES F, CALARCO J P, MARTIENSSEN R A. Reprogramming the epigenome in Arabidopsis pollen [J]. Cold Spring Harb Symp Quant Biol, 2012, 77: 1-5.
[183]SOPPE W J, JACOBSEN S E, ALONSO-BLANCO C, et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene [J]. Mol Cell, 2000, 6(4): 791-802.
[184]WALKER J, GAO H, ZHANG J, et al. Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis [J]. Nat Genet, 2018, 50(1): 130-7.
[185]CALARCO J P, BORGES F, DONOGHUE M T, et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA [J]. Cell, 2012, 151(1): 194-205.
[186]ZEMACH A, MCDANIEL I E, SILVA P, et al. Genome-wide evolutionary analysis of eukaryotic DNA methylation [J]. Science, 2010, 328(5980): 916-9.
[187]SLOTKIN R K, VAUGHN M, BORGES F, et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen [J]. Cell, 2009, 136(3): 461-72.
[188]DU J, JOHNSON L M, JACOBSEN S E, et al. DNA methylation pathways and their crosstalk with histone methylation [J]. Nat Rev Mol Cell Biol, 2015, 16(9): 519-32.
[189]BERRY S, DEAN C. Environmental perception and epigenetic memory: mechanistic insight through FLC [J]. Plant J, 2015, 83(1): 133-48.
[190]COSTA S, DEAN C. Storing memories: the distinct phases of Polycomb-mediated silencing of Arabidopsis FLC [J]. Biochem Soc Trans, 2019, 47(4): 1187-96.
[191]CREVILLEN P, YANG H, CUI X, et al. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state [J]. Nature, 2014, 515(7528): 587-90.
[192]TAO Z, SHEN L, GU X, et al. Embryonic epigenetic reprogramming by a pioneer transcription factor in plants [J]. Nature, 2017, 551(7678): 124-8.
[193]SHELDON C C, HILLS M J, LISTER C, et al. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization [J]. Proc Natl Acad Sci U S A, 2008, 105(6): 2214-9.
[194]XU G, TAO Z, HE Y. Embryonic reactivation of FLOWERING LOCUS C by ABSCISIC ACID-INSENSITIVE 3 establishes the vernalization requirement in each Arabidopsis generation [J]. Plant Cell, 2022, 34(6): 2205-21.
[195]LUO X, OU Y, LI R, et al. Maternal transmission of the epigenetic 'memory of winter cold' in Arabidopsis [J]. Nat Plants, 2020, 6(10): 1211-8.
[196]ZHAO F, ZHANG H, 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): 2051-63.
[197]HUANG X, SUN M X. H3K27 methylation regulates the fate of two cell lineages in male gametophytes [J]. Plant Cell, 2022, 34(8): 2989-3005.
[198]BORGES F, GOMES G, GARDNER R, et al. Comparative transcriptomics of Arabidopsis sperm cells [J]. Plant Physiol, 2008, 148(2): 1168-81.
[199]BORG M, PAPAREDDY R K, DOMBEY R, et al. Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis [J]. Elife, 2021, 10.
[200]ROTMAN N, DURBARRY A, WARDLE A, et al. A novel class of MYB factors controls sperm-cell formation in plants [J]. Curr Biol, 2005, 15(3): 244-8.
[201]YAMAOKA S, NISHIHAMA R, YOSHITAKE Y, et al. Generative cell specification requires transcription factors evolutionarily conserved in land plants [J]. Curr Biol, 2018, 28(3): 479-86 e5.
[202]OH S A, HOAI T N T, PARK H J, et al. MYB81, a microspore-specific GAMYB transcription factor, promotes pollen mitosis I and cell lineage formation in Arabidopsis [J]. Plant J, 2020, 101(3): 590-603.
[203]VERELST W, SAEDLER H, MUNSTER T. MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters [J]. Plant Physiol, 2007, 143(1): 447-60.
[204]VERELST W, TWELL D, DE FOLTER S, et al. MADS-complexes regulate transcriptome dynamics during pollen maturation [J]. Genome Biol, 2007, 8(11): R249.
[205]FENG X, ZILBERMAN D, DICKINSON H. A conversation across generations: soma-germ cell crosstalk in plants [J]. Dev Cell, 2013, 24(3): 215-25.
[206]SEGUI-SIMARRO J M, NUEZ F. How microspores transform into haploid embryos: changes associated with embryogenesis induction and microspore-derived embryogenesis [J]. Physiol Plant, 2008, 134(1): 1-12.
[207]LI H, SORIANO M, CORDEWENER J, et al. The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte [J]. Plant Cell, 2014, 26(1): 195-209.
[208]HEARD E, MARTIENSSEN R A. Transgenerational epigenetic inheritance: myths and mechanisms [J]. Cell, 2014, 157(1): 95-109.
[209]FENG S, JACOBSEN S E, REIK W. Epigenetic reprogramming in plant and animal development [J]. Science, 2010, 330(6004): 622-7.
[210]BAULCOMBE D C, DEAN C. Epigenetic regulation in plant responses to the environment [J]. Cold Spring Harb Perspect Biol, 2014, 6(9): a019471.
[211]GEHRING M. Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming? [J]. New Phytol, 2019, 224(1): 91-6.
[212]SANTOS M R, BISPO C, BECKER J D. Isolation of Arabidopsis pollen, sperm cells, and vegetative nuclei by fluorescence-activated cell sorting (FACS) [J]. Methods Mol Biol, 2017, 1669: 193-210.
[213]BORGES F, GARDNER R, LOPES T, et al. FACS-based purification of Arabidopsis microspores, sperm cells and vegetative nuclei [J]. Plant Methods, 2012, 8(1): 44.
[214]ZHENG J, YE Y, XU Q, et al. A Modified SMART-Seq Method for Single-Cell Transcriptomic Analysis of Embryoid Body Differentiation [J]. Methods Mol Biol, 2022, 2520: 233-59.
[215]CHEN S, ZHOU Y, CHEN Y, et al. fastp: an ultra-fast all-in-one FASTQ preprocessor [J]. Bioinformatics, 2018, 34(17): i884-i90.
[216]CHEN C, KHALEEL S S, HUANG H, et al. Software for pre-processing Illumina next-generation sequencing short read sequences [J]. Source Code Biol Med, 2014, 9: 8.
[217]BOLGER A M, LOHSE M, USADEL B. Trimmomatic: a flexible trimmer for Illumina sequence data [J]. Bioinformatics, 2014, 30(15): 2114-20.
[218]PAN Y, WANG X, LIU L, et al. Whole genome mapping with feature sets from high-throughput sequencing data [J]. PLoS One, 2016, 11(9): e0161583.
[219]LANGMEAD B, SALZBERG S L. Fast gapped-read alignment with Bowtie2 [J]. Nat Methods, 2012, 9(4): 357-9.
[220]LANGMEAD B, TRAPNELL C, POP M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome [J]. Genome Biol, 2009, 10(3): R25.
[221]KIM D, PERTEA G, TRAPNELL C, et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions [J]. Genome Biol, 2013, 14(4): R36.
[222]KIM D, PAGGI J M, PARK C, et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype [J]. Nat Biotechnol, 2019, 37(8): 907-15.
[223]DOBIN A, DAVIS C A, SCHLESINGER F, et al. STAR: ultrafast universal RNA-seq aligner [J]. Bioinformatics, 2013, 29(1): 15-21.
[224]TRAPNELL C, WILLIAMS B A, PERTEA G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation [J]. Nat Biotechnol, 2010, 28(5): 511-5.
[225]TRAPNELL C, ROBERTS A, GOFF L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks [J]. Nat Protoc, 2012, 7(3): 562-78.
[226]YU G, WANG L G, HAN Y, et al. clusterProfiler: an R package for comparing biological themes among gene clusters [J]. OMICS, 2012, 16(5): 284-7.
[227]ASHBURNER M, BALL C A, BLAKE J A, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium [J]. Nat Genet, 2000, 25(1): 25-9.
[228]KANEHISA M, GOTO S, SATO Y, et al. Data, information, knowledge and principle: back to metabolism in KEGG [J]. Nucleic Acids Res, 2014, 42(Database issue): D199-205.
[229]ZHANG Y, LIU T, MEYER C A, et al. Model-based analysis of ChIP-Seq (MACS) [J]. Genome Biol, 2008, 9(9): R137.
[230]HEINZ S, BENNER C, SPANN N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities [J]. Mol Cell, 2010, 38(4): 576-89.
[231]NAVARRO GONZALEZ J, ZWEIG A S, SPEIR M L, et al. The UCSC genome browser database: 2021 update [J]. Nucleic Acids Res, 2021, 49(D1): D1046-D57.
[232]ROBINSON J T, THORVALDSDOTTIR H, WINCKLER W, et al. Integrative genomics viewer [J]. Nat Biotechnol, 2011, 29(1): 24-6.
[233]LOPEZ-DELISLE L, RABBANI L, WOLFF J, et al. pyGenomeTracks: reproducible plots for multivariate genomic datasets [J]. Bioinformatics, 2021, 37(3): 422-3.
[234]QUINLAN A R, HALL I M. BEDTools: a flexible suite of utilities for comparing genomic features [J]. Bioinformatics, 2010, 26(6): 841-2.
[235]KAMINOW B, YUNUSOV D, DOBIN A. STARsolo: accurate, fast and versatile mapping/quantification of single-cell and single-nucleus RNA-seq data [J]. bioRxiv, 2021.
[236]HAO Y, HAO S, ANDERSEN-NISSEN E, et al. Integrated analysis of multimodal single-cell data [J]. Cell, 2021, 184(13): 3573-87 e29.
[237]TREMOUSAYGUE D, GARNIER L, BARDET C, et al. Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells [J]. Plant J, 2003, 33(6): 957-66.
[238]BORG M, BROWNFIELD L, KHATAB H, et al. The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis [J]. Plant Cell, 2011, 23(2): 534-49.
[239]RADA-IGLESIAS A, BAJPAI R, SWIGUT T, et al. A unique chromatin signature uncovers early developmental enhancers in humans [J]. Nature, 2011, 470(7333): 279-83.
[240]WHYTE W A, ORLANDO D A, HNISZ D, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes [J]. Cell, 2013, 153(2): 307-19.
[241]XIANG Y, ZHANG Y, XU Q, et al. Epigenomic analysis of gastrulation identifies a unique chromatin state for primed pluripotency [J]. Nat Genet, 2020, 52(1): 95-105.
[242]GU Y, RASMUSSEN C G. Cell biology of primary cell wall synthesis in plants [J]. Plant Cell, 2022, 34(1): 103-28.
[243]LAFON-PLACETTE C, KOHLER C. Embryo and endosperm, partners in seed development [J]. Curr Opin Plant Biol, 2014, 17: 64-9.
[244]JUNG Y H, SAURIA M E G, LYU X, et al. Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes [J]. Cell Rep, 2017, 18(6): 1366-82.
[245]LESCH B J, SILBER S J, MCCARREY J R, et al. Parallel evolution of male germline epigenetic poising and somatic development in animals [J]. Nat Genet, 2016, 48(8): 888-94.
[246]WEINHOFER I, HEHENBERGER E, ROSZAK P, et al. H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation [J]. PLoS Genet, 2010, 6(10).
[247]YANOFSKY M F, MA H, BOWMAN J L, et al. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors [J]. Nature, 1990, 346(6279): 35-9.
[248]GOTO K, MEYEROWITZ E M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA [J]. Genes Dev, 1994, 8(13): 1548-60.
[249]PELAZ S, DITTA G S, BAUMANN E, et al. B and C floral organ identity functions require SEPALLATA MADS-box genes [J]. Nature, 2000, 405(6783): 200-3.
[250]BOWMAN J L, SMYTH D R, MEYEROWITZ E M. The ABC model of flower development: then and now [J]. Development, 2012, 139(22): 4095-8.
[251]SHI X, SUN X, ZHANG Z, et al. GLUCAN SYNTHASE-LIKE 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice [J]. Plant Cell Physiol, 2015, 56(3): 497-509.
[252]ENNS L C, KANAOKA M M, TORII K U, et al. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility [J]. Plant Mol Biol, 2005, 58(3): 333-49.
[253]GAZZARRINI S, TSUCHIYA Y, LUMBA S, et al. The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid [J]. Dev Cell, 2004, 7(3): 373-85.
[254]ZHAO C, AVCI U, GRANT E H, et al. XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem [J]. Plant J, 2008, 53(3): 425-36.
[255]LIU J, SHENG L, XU Y, et al. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis [J]. Plant Cell, 2014, 26(3): 1081-93.
[256]REIK W, DEAN W, WALTER J. Epigenetic reprogramming in mammalian development [J]. Science, 2001, 293(5532): 1089-93.
[257]BRAUN R E. Packaging paternal chromosomes with protamine [J]. Nat Genet, 2001, 28(1): 10-2.
[258]HAMMOUD S S, NIX D A, ZHANG H, et al. Distinctive chromatin in human sperm packages genes for embryo development [J]. Nature, 2009, 460(7254): 473-8.
[259]CARONE B R, HUNG J H, HAINER S J, et al. High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm [J]. Dev Cell, 2014, 30(1): 11-22.
[260]SAMANS B, YANG Y, KREBS S, et al. Uniformity of nucleosome preservation pattern in Mammalian sperm and its connection to repetitive DNA elements [J]. Dev Cell, 2014, 30(1): 23-35.
[261]GE Z, BERGONCI T, ZHAO Y, et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling [J]. Science, 2017, 358(6370): 1596-600.
[262]BOISSON-DERNIER A, ROY S, KRITSAS K, et al. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge [J]. Development, 2009, 136(19): 3279-88.
[263]MIYAZAKI S, MURATA T, SAKURAI-OZATO N, et al. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization [J]. Curr Biol, 2009, 19(15): 1327-31.
[264]CHEN K, CHEN Z, WU D, et al. Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes [J]. Nat Genet, 2015, 47(10): 1149-57.
[265]DAHL J A, JUNG I, AANES H, et al. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition [J]. Nature, 2016, 537(7621): 548-52.
[266]ZHANG B, ZHENG H, HUANG B, et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development [J]. Nature, 2016, 537(7621): 553-7.
[267]LIU X, WANG C, LIU W, et al. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos [J]. Nature, 2016, 537(7621): 558-62.
[268]BELHOCINE M, SIMONIN M, ABAD FLORES J D, et al. Dynamics of broad H3K4me3 domains uncover an epigenetic switch between cell identity and cancer-related genes [J]. Genome Res, 2022, 32(7): 1328-42.
[269]MONTGOMERY S A, TANIZAWA Y, GALIK B, et al. Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin [J]. Curr Biol, 2020, 30(4): 573-88 e7.
[270]VOIGT P, LEROY G, DRURY W J, 3RD, et al. Asymmetrically modified nucleosomes [J]. Cell, 2012, 151(1): 181-93.
[271]YUAN L, SONG X, ZHANG L, et al. The transcriptional repressors VAL1 and VAL2 recruit PRC2 for genome-wide Polycomb silencing in Arabidopsis [J]. Nucleic Acids Res, 2021, 49(1): 98-113.
[272]YAN W, CHEN D, SMACZNIAK C, et al. Dynamic and spatial restriction of Polycomb activity by plant histone demethylases [J]. Nat Plants, 2018, 4(9): 681-9.
[273]HOFMANN F, SCHON M A, NODINE M D. The embryonic transcriptome of Arabidopsis thaliana [J]. Plant Reprod, 2019, 32(1): 77-91.