Chromatin remodelling during male gametophyte development

Plant Journal

Volumn 83, Issue 1, 2015, Pages 177-188

  Borg, Michael ^a   Berger, Frédéric ^a  

^a Vienna Biocenter   (Austria)

Author keywords

chromatin; epigenetics; histone variants; male gametophyte; pollen; sperm cells

Indexed keywords

CHROMOSOMES; LIFE CYCLE; PLANTS (BOTANY);

CHROMATIN; EPIGENETICS; HISTONE VARIANTS; MALE GAMETOPHYTES; POLLEN; SPERM CELLS;

CYTOLOGY;

CHROMATIN; HISTONE;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLOIDY; METABOLISM; PHYSIOLOGY; POLLEN;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLOWERS; HAPLOIDY; HISTONES; POLLEN;

EID: 84932194258     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12856     Document Type: Article

References (127)

1. Abdelsamad, A., and, Pecinka, A., (2014) Pollen-specific activation of Arabidopsis retrogenes is associated with global transcriptional reprogramming. Plant Cell, 26, 3299-3313.
2. Akiyama, T., Suzuki, O., Matsuda, J., and, Aoki, F., (2011) Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet. 7, e1002279.
3. Anderson, S.N., Johnson, C.S., Jones, D.S., Conrad, L.J., Gou, X., Russell, S.D., and, Sundaresan, V., (2013) Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization. Plant J. 76, 729-741.
4. Aw, S.J., Hamamura, Y., Chen, Z., Schnittger, A., and, Berger, F., (2010) Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development, 137, 2683-2690.
5. Balaji, S., Iyer, L.M., and, Aravind, L., (2009) HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol. BioSyst. 5, 269-275.
6. Berger, F., and, Twell, D., (2011) Germline specification and function in plants. Annu. Rev. Plant Biol. 62, 461-484.
7. Berger, S.L., (2007) The complex language of chromatin regulation during transcription. Nature, 447, 407-412.
8. Bernad, R., Sánchez, P., Rivera, T., et al. (2011) Xenopus HJURP and condensin II are required for CENP-A assembly. J. Cell Biol. 192, 569-582.
9. Black, B.E., and, Bassett, E.A., (2008) The histone variant CENP-A and centromere specification. Curr. Opin. Cell Biol. 20, 91-100.
10. Bonnefoy, E., Orsi, G.A., Couble, P., and, Loppin, B., (2007) The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet. 3, 1991-2006.
11. Borg, M., Brownfield, L., Khatab, H., Sidorova, A., Lingaya, M., and, Twell, D., (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell, 23, 534-549.
12. Borg, M., Brownfield, L., and, Twell, D., (2009) Male gametophyte development: a molecular perspective. J. Exp. Bot. 60, 1465-1478.
13. Borg, M., Rutley, N., Kagale, S., et al. (2014) An EAR-dependent regulatory module promotes male germ cell division and sperm fertility in Arabidopsis. Plant Cell, 26, 2098-2113.
14. Borg, M., and, Twell, D., (2010) Life after meiosis: patterning the angiosperm male gametophyte. Biochem. Soc. Trans. 38, 577-582.
15. Borges, F., Calarco, J.P., and, Martienssen, R.A., (2012) Reprogramming the epigenome in Arabidopsis pollen. Cold Spring Harb. Symp. Quant. Biol. 77, 1-5.
16. Borges, F., Gomes, G., Gardner, R., Moreno, N., McCormick, S., Feijõ, J.A., and, Becker, J.D., (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148, 1168-1181.
17. Boskovic, A., and, Torres-Padilla, M.-E., (2013) How mammals pack their sperm: a variant matter. Genes Dev. 27, 1635-1639.
18. Boussouar, F., Rousseaux, S., and, Khochbin, S., (2008) A new insight into male genome reprogramming by histone variants and histone code. Cell Cycle, 7, 3499-3502.
19. Brown, D.T., (2001) Histone variants: are they functionally heterogeneous? Genome Biol. 2, REVIEWS0006.
20. Brownfield, L., Hafidh, S., Borg, M., Sidorova, A., Mori, T., and, Twell, D., (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. G. P. Copenhaver, ed. PLoS Genet. 5, e1000430.
21. Brykczynska, U., Hisano, M., Erkek, S., et al. (2010) Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687.
22. Cartagena, J.A., Matsunaga, S., Seki, M., et al. (2008) The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev. Biol. 315, 355-368.
23. Chen, Z., Tan, J.L.H., Ingouff, M., Sundaresan, V., and, Berger, F., (2008) Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana. Development, 135, 65-73.
24. de Graaf, B.H.J., de Derksen, J.W.M., and, Mariani, C., (2001) Pollen and pistil in the progamic phase. Sex. Plant Reprod. 14, 41-55.
25. Drabent, B., Saftig, P., Bode, C., and, Doenecke, D., (2000) Spermatogenesis proceeds normally in mice without linker histone H1t. Histochem. Cell Biol. 113, 433-442.
26. Dunleavy, E.M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y., and, Almouzni-Pettinotti, G., (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell, 137, 485-497.
27. Durbarry, A., Vizir, I., and, Twell, D., (2005) Male germ line development in Arabidopsis: duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol. 137, 297-307.
28. Elsässer, S.J., Huang, H., Lewis, P.W., Chin, J.W., Allis, C.D., and, Patel, D.J., (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature, 491, 560-565.
29. Erenpreiss, J., Spano, M., Erenpreisa, J., Bungum, M., and, Giwercman, A., (2006) Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J. Androl. 8, 11-29.
30. Erhardt, S., Mellone, B.G., Betts, C.M., Zhang, W., Karpen, G.H., and, Straight, A.F., (2008) Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J. Cell Biol. 183, 805-818.
31. Feng, S., Jacobsen, S.E., and, Reik, W., (2010) Epigenetic reprogramming in plant and animal development. Science, 330, 622-627.
32. Feng, X., Zilberman, D., and, Dickinson, H., (2013) A conversation across generations: soma-germ cell crosstalk in plants. Dev. Cell, 24, 215-225.
33. Filipescu, D., Szenker, E., and, Almouzni, G., (2013) Developmental roles of histone H3 variants and their chaperones. Trends Genet. 29, 630-640.
34. Foltz, D.R., Jansen, L.E.T., Bailey, A.O., Yates, J.R., Bassett, E.A., Wood, S., Black, B.E., and, Cleveland, D.W., (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell, 137, 472-484.
35. Friedman, W.E., (1999) Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development, 126, 1065-1075.
36. Gomendio, M., Malo, A.F., Garde, J., and, Roldan, E.R.S., (2007) Sperm traits and male fertility in natural populations. Reproduction, 134, 19-29.
37. Grant-Downton, R., Kourmpetli, S., Hafidh, S., Khatab, H., Le Trionnaire, G., Dickinson, H., and, Twell, D., (2013) Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr. Biol. 23, R599-R601.
38. Gurard-Levin, Z.A., Quivy, J.-P., and, Almouzni, G., (2014) Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83, 487-517.
39. Gutierrez-Marcos, J.F., and, Dickinson, H.G., (2012) Epigenetic reprogramming in plant reproductive lineages. Plant Cell Physiol. 53, 817-823.
40. Guyon, V.N., Astwood, J.D., Garner, E.C., Dunker, A.K., and, Taylor, L.P., (2000) Isolation and characterization of cDNAs expressed in the early stages of flavonol-induced pollen germination in petunia. Plant Physiol. 123, 699-710.
41. Hadj-Mabrouk, H., Kader, J.C., and, Robert, D., (1979) Les protéines basiques du noyau du spermatozoide de l'Equisetum arvense L. Etude par Electrophor. CR Acad. Sci. Paris, 289, 969-972.
42. Hammoud, S.S., Nix, D.A., Zhang, H., Purwar, J., Carrell, D.T., and, Cairns, B.R., (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature, 460, 473-478.
43. Hayashi, K., de Sousa Lopes, S.M.C., and, Surani, M.A., (2007) Germ cell specification in mice. Science, 316, 394-396.
44. Henikoff, S., and, Furuyama, T., (2012) The unconventional structure of centromeric nucleosomes. Chromosoma, 121, 341-352.
45. Henikoff, S., Furuyama, T., and, Ahmad, K., (2004) Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet. 20, 320-326.
46. Hennig, L., Taranto, P., Walser, M., Schönrock, N., and, Gruissem, W., (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development, 130, 2555-2565.
47. Hoffmann, R.D., and, Palmgren, M.G., (2013) Epigenetic repression of male gametophyte-specific genes in the Arabidopsis sporophyte. Mol. Plant, 6, 1176-1186.
48. Honys, D., and, Twell, D., (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85.
49. Houben, A., Kumke, K., Nagaki, K., and, Hause, G., (2011) CENH3 distribution and differential chromatin modifications during pollen development in rye (Secale cereale L.). Chromosome Res. 19, 471-480.
50. Ibarra, C.A., Feng, X., Schoft, V.K., et al. (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science, 337, 1360-1364.
51. Ingouff, M., and, Berger, F., (2010) Histone3 variants in plants. Chromosoma, 119, 27-33.
52. Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T., and, Berger, F., (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17, 1032-1037.
53. Ingouff, M., Rademacher, S., Holec, S., et al. (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20, 2137-2143.
54. Johnson, G.D., Lalancette, C., Linnemann, A.K., Leduc, F., Boissonneault, G., and, Krawetz, S.A., (2011) The sperm nucleus: chromatin, RNA, and the nuclear matrix. Reproduction, 141, 21-36.
55. Johnson, L., Mollah, S., Garcia, B.A., Muratore, T.L., Shabanowitz, J., Hunt, D.F., and, Jacobsen, S.E., (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res. 32, 6511-6518.
56. Jukes, T.H., and, Cantor, C.R., (1969) Evolution of protein molecules. Mamm. Protein Metab. 3, 21-132.
57. Juliano, C., and, Wessel, G., (2010) Developmental biology. Versatile germline genes. Science, 329, 640-641.
58. Kawashima, T., and, Berger, F., (2014) Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15, 613-624.
59. Kaya, H., Shibahara, K., Taoka, K., Iwabuchi, M., Stillman, B., and, Araki, T., (2001) FASCIATA Genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell, 104, 131-142.
60. Konev, A.Y., Tribus, M., Park, S.Y., et al. (2007) CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science, 317, 1087-1090.
61. Kwiatkowska, M., Kaźmierczak, A., and, Popłońska, K., (2002) Ultrastructural, autoradiographic and electrophoretic examinations of Chara tomentosa spermiogenesis. Acta Soc. Bot. Pol. 71, 201-209.
62. Lin, Q., Sirotkin, A., and, Skoultchi, A.I., (2000) Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Mol. Cell. Biol. 20, 2122-2128.
63. Loppin, B., Bonnefoy, E., Anselme, C., Laurençon, A., Karr, T.L., and, Couble, P., (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature, 437, 1386-1390.
64. Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F., and, Richmond, T.J., (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 389, 251-260.
65. Maze, I., Noh, K.-M., Soshnev, A.A., and, Allis, C.D., (2014) Every amino acid matters: essential contributions of histone variants to mammalian development and disease. Nat. Rev. Genet. 15, 259-271.
66. Meistrich, M.L., Mohapatra, B., Shirley, C.R., and, Zhao, M., (2003) Roles of transition nuclear proteins in spermiogenesis. Chromosoma, 111, 483-488.
67. Mellone, B.G., Grive, K.J., Shteyn, V., Bowers, S.R., Oderberg, I., and, Karpen, G.H., (2011) Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet. 7, e1002068.
68. Mérai, Z., Chumak, N., García-Aguilar, M., et al. (2014) The AAA-ATPase molecular chaperone Cdc48/p97 disassembles sumoylated centromeres, decondenses heterochromatin, and activates ribosomal RNA genes. Proc. Natl Acad. Sci. USA, 111, 16166-16171.
69. Mito, Y., Henikoff, J.G., and, Henikoff, S., (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37, 1090-1097.
70. Mizukami, I., and, Gall, J., (1966) Centriole replication: II. Sperm formation in the fern, Marsilea, and the cycad, Zamia. J. Cell Biol. 29, 97-111.
71. Montellier, E., Boussouar, F., Rousseaux, S., et al. (2013) Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 27, 1680-1692.
72. Moree, B., Meyer, C.B., Fuller, C.J., and, Straight, A.F., (2011) CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J. Cell Biol. 194, 855-871.
73. Nie, M., Aslanian, A., Prudden, J., Heideker, J., Vashisht, A.A., Wohlschlegel, J.A., Yates, J.R., and, Boddy, M.N., (2012) Dual recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in SUMO-targeted ubiquitin ligase-mediated genome stability functions. J. Biol. Chem. 287, 29610-29619.
74. Nie, X., Wang, H., Li, J., Holec, S., and, Berger, F., (2014) The HIRA complex that deposits the histone H3.3 is conserved in Arabidopsis and facilitates transcriptional dynamics. Biol. Open, 3, 794-802.
75. Oakeley, E.J., Podesta, A., and, Jost, J.-P., (1997) Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc. Natl Acad. Sci. 94, 11721-11725.
76. Okada, T., Endo, M., Singh, M.B., and, Bhalla, P.L., (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J. 44, 557-568.
77. Okada, T., Singh, M.B., and, Bhalla, P.L., (2006) Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol. Biol. 62, 503-512.
78. Ooi, S.L., Priess, J.R., and, Henikoff, S., (2006) Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. S. Mango, ed. PLoS Genet. 2, e97.
79. Orsi, G.A., Algazeery, A., Meyer, R.E., et al. (2013) Drosophila Yemanuclein and HIRA cooperate for de novo assembly of H3.3-containing nucleosomes in the male pronucleus. PLoS Genet. 9, e1003285.
80. Palovaara, J., Saiga, S., and, Weijers, D., (2013) Transcriptomics approaches in the early Arabidopsis embryo. Trends Plant Sci. 18, 514-521.
81. Pandey, P., Houben, A., Kumlehn, J., Melzer, M., and, Rutten, T., (2013) Chromatin alterations during pollen development in Hordeum vulgare. Cytogenet. Genome Res. 141, 50-57.
82. Pillot, M., Autran, D., Leblanc, O., and, Grimanelli, D., (2010) A role for CHROMOMETHYLASE3 in mediating transposon and euchromatin silencing during egg cell reprogramming in Arabidopsis. Plant Signal. Behav. 5, 1167-1170.
83. Prymakowska-Bosak, M., (1999) Linker histones play a role in male meiosis and the development of pollen grains in tobacco. Plant Cell Online, 11, 2317-2330.
84. Qin, Y., Leydon, A.R., Manziello, A., Pandey, R., Mount, D., Denic, S., Vasic, B., Johnson, M.A., and, Palanivelu, R., (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet. 5, e1000621.
85. Quint, M., Drost, H.-G., Gabel, A., Ullrich, K.K., Bönn, M., and, Grosse, I., (2012) A transcriptomic hourglass in plant embryogenesis. Nature, 490, 98-101.
86. Ramirez-Parra, E., and, Gutierrez, C., (2007) The many faces of chromatin assembly factor 1. Trends Plant Sci. 12, 570-576.
87. Rathke, C., Barckmann, B., Burkhard, S., Jayaramaiah-Raja, S., Roote, J., and, Renkawitz-Pohl, R., (2010) Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis. Eur. J. Cell Biol. 89, 326-338.
88. Ray-Gallet, D., Quivy, J.-P., Scamps, C., Martini, E.M.-D., Lipinski, M., and, Almouzni, G., (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell, 9, 1091-1100.
89. Reynolds, W.F., and, Wolfe, S.L., (1978) Changes in basic proteins during sperm maturation in a plant, Marchantia polymorpha. Exp. Cell Res. 116, 269-273.
90. Reynolds, W.F., and, Wolfe, S.L., (1984) Protamines in plant sperm. Exp. Cell Res. 152, 443-448.
91. Ribeiro, T., Viegas, W., and, Morais-Cecílio, L., (2009) Epigenetic marks in the mature pollen of Quercus suber L. (Fagaceae). Sex. Plant Reprod. 22, 1-7.
92. Robert, D., (1984) Le noyau du gamète mâle chez les végétaux. Ann. des Sci. Nat. Bot. Biol. Végétale, 6, 151-164.
93. Robert, D., Blaize-Sauvanet, A., Hadj-Mabrouk, H., and, Khlifi, S., (1986) Nuclear organization in the motile male gamete of the fern Scolopendrium vulgare. J. Submicrosc. Cytol. 18, 349-359.
94. Rotman, N., Durbarry, A., Wardle, A., Yang, W.C., Chaboud, A., Faure, J.E., Berger, F., and, Twell, D., (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol. 15, 244-248.
95. Rousseaux, S., Caron, C., Govin, J., Lestrat, C., Faure, A.-K., and, Khochbin, S., (2005) Establishment of male-specific epigenetic information. Gene, 345, 139-153.
96. Russell, S.D., Gou, X., Wong, C.E., Wang, X., Yuan, T., Wei, X., Bhalla, P.L., and, Singh, M.B., (2012) Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol. 195, 560-573.
97. Rutley, N., and, Twell, D., (2015) A decade of pollen transcriptomics. Plant Reprod. 28, 73-89.
98. Sano, Y., and, Tanaka, I., (2005) A histone H3.3-like gene specifically expressed in the vegetative cell of developing lily pollen. Plant Cell Physiol. 46, 1299-1308.
99. Sano, Y., and, Tanaka, I., (2010) Distinct localization of histone H3 methylation in the vegetative nucleus of lily pollen. Cell Biol. Int. 34, 253-259.
100. Santenard, A., and, Torres-Padilla, M.-E., (2009) Epigenetic reprogramming in mammalian reproduction: contribution from histone variants. Epigenetics, 4, 80-84.
101. Sassone-Corsi, P., (2002) Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science, 296, 2176-2178.
102. Sawatsubashi, S., Murata, T., Lim, J., et al. (2010) A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev. 24, 159-170.
103. Schmidt, A., Wuest, S.E., Vijverberg, K., Baroux, C., Kleen, D., and, Grossniklaus, U., (2011) Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9, e1001155.
104. Schoft, V.K., Chumak, N., Mosiolek, M., Slusarz, L., Komnenovic, V., Brownfield, L., Twell, D., Kakutani, T., and, Tamaru, H., (2009) Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 10, 1015-1021.
105. Schümperli, D., (1986) Cell-cycle regulation of histone gene expression. Cell, 45, 471-472.
106. Sharp, L.W., (1914) Spermatogenesis in Marsilia. Bot. Gaz. 58, 419-431.
107. Slotkin, R.K., Vaughn, M., Borges, F., Tanurdžic, M., Becker, J.D., Feijõ, J.A., and, Martienssen, R.A., (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell, 136, 461-472.
108. Smith, S., and, Stillman, B., (1989) Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell, 58, 15-25.
109. Stoler, S., Rogers, K., Weitze, S., Morey, L., Fitzgerald-Hayes, M., and, Baker, R.E., (2007) Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl Acad. Sci. USA, 104, 10571-10576.
110. Strome, S., and, Lehmann, R., (2007) Germ versus soma decisions: lessons from flies and worms. Science, 316, 392-393.
111. Stroud, H., Otero, S., Desvoyes, B., Ramírez-Parra, E., Jacobsen, S.E., and, Gutierrez, C., (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 109, 5370-5375.
112. Swanson, W.J., and, Vacquier, V.D., (2002) The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137-144.
113. Tagami, H., Ray-Gallet, D., Almouzni, G., and, Nakatani, Y., (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell, 116, 51-61.
114. Talbert, P.B., Ahmad, K., Almouzni, G., et al. (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin, 5, 7.
115. Tanaka, I., Ono, K., and, Fukuda, T., (1998) The developmental fate of angiosperm pollen is associated with a preferential decrease in the level of histone H1 in the vegetative nucleus. Planta, 206, 561-569.
116. Torres-Padilla, M.-E., Bannister, A.J., Hurd, P.J., Kouzarides, T., and, Zernicka-Goetz, M., (2006) Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 50, 455-461.
117. Ueda, K., Kinoshita, Y., Xu, Z.J., Ide, N., Ono, M., Akahori, Y., Tanaka, I., and, Inoue, M., (2000) Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum. Chromosoma, 108, 491-500.
118. Ueda, K., Suzuki, M., Ono, M., Ide, N., Tanaka, I., and, Inoue, M., (2005) Male gametic cell-specific histone gH2A gene of Lilium longiflorum: genomic structure and promoter activity in the generative cell. Plant Mol. Biol. 59, 229-238.
119. Ueda, K., and, Tanaka, I., (1995) Male gametic nucleus-specific H2B and H3 histones, designated gH2B and gH3, in Lilium longiflorum. Planta, 197, 289-295.
120. Ueda, K., and, Tanaka, I., (1994) The basic proteins of male gametic nuclei isolated from pollen grains of Lilium longiflorum. Planta, 192, 446-452.
121. Wirbelauer, C., Bell, O., and, Schübeler, D., (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 19, 1761-1766.
122. Wolffe, A.P., (1999) Chromatin: Structure and Function (Google eBook). London: Academic Press.
123. Wollmann, H., Holec, S., Alden, K., Clarke, N.D., Jacques, P.-É., and, Berger, F., (2012) Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLoS Genet. 8, e1002658.
124. Wu, S.-F., Zhang, H., and, Cairns, B.R., (2011) Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res. 21, 578-589.
125. Wykes, S.M., and, Krawetz, S.A., (2003) The structural organization of sperm chromatin. J. Biol. Chem. 278, 29471-29477.
126. Xu, H., Swoboda, I., Bhalla, P.L., and, Singh, M.B., (1999) Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol. Biol. 39, 607-614.
127. Zentner, G.E., and, Henikoff, S., (2013) Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 20, 259-266.