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Canonical Histones and Their Variants in Plants: Evolution and Functions

  • Marlon S. Zambrano-Mila
  • Maria J. Aldaz-Villao
  • Juan Armando Casas-Mollano
Chapter

Abstract

The DNA found inside the nuclei of eukaryotic cells is complexed with histone proteins forming the polymer called chromatin. Chromatin is organized into repeating units, nucleosomes, which are comprised of DNA wrapped around an octamer of the core histones H2A, H2B, H3, and H4. Histones are encoded by multigene families organized as clusters in animals and algae, but as dispersed copies in the genome of higher plants. The bulk of histones are expressed during the S-phase of the cell cycle in order for them to be incorporated into the chromatin of the newly replicated DNA. In addition to these canonical histones, eukaryotic genomes also encode related histone variants. Histone variants are expressed independently of the cell cycle and replace canonical histones when chromatin is disrupted by processes such as transcription, DNA repair, recombination, etc. This chapter will review the core histone families H2A, H2B, H3, and H4 in higher plants. For each family, canonical histones and their variants will be described emphasizing their evolutionary origin and the roles they play in different chromatin-mediated processes. In the plant kingdom, the core histones families have diversified allowing some isoforms to maintain their original roles, but also the emergence of new variants with novel functions. Both conserved and plant-specific histone variants participate in all aspects of plant life including development, phase transitions, flowering, responses to abiotic stresses, and germline formation among others. Many of the processes regulated by histones involve agronomically important traits highlighting their potential as targets for crop breeding and biotechnology.

Keywords

Chromatin Canonical histones Histone variants H3.3 CENH3 H2A.Z H2A.X H2A.W gH2B gH4 

Notes

Acknowledgments

We would like to acknowledge the support of the School of Biological Sciences and Engineering during the preparation of the manuscript. JAC-M research is supported, in part, by a startup grant from Yachay Tech University. We apologize to all researchers whose contributions could not be cited because of space limitations.

References

  1. Arents G, Moudrianakis EN (1995) The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci U S A 92(24):11170–11174CrossRefGoogle Scholar
  2. Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN (1991) The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A 88(22):10148–10152CrossRefGoogle Scholar
  3. Aul RB, Oko RJ (2002) The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev Biol 242(2):376–387CrossRefGoogle Scholar
  4. Benoit M, Simon L, Desset S, Duc C, Cotterell S, Poulet A, Le Goff S, Tatout C, Probst AV (2018) Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development. New Phytol.  https://doi.org/10.1111/nph.15248CrossRefGoogle Scholar
  5. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447(7143):407–412.  https://doi.org/10.1038/nature05915CrossRefGoogle Scholar
  6. Bergmuller E, Gehrig PM, Gruissem W (2007) Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J Proteome Res 6(9):3655–3668.  https://doi.org/10.1021/pr0702159CrossRefPubMedGoogle Scholar
  7. Blower MD, Karpen GH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3(8):730–739.  https://doi.org/10.1038/35087045CrossRefPubMedPubMedCentralGoogle Scholar
  8. Blower MD, Daigle T, Kaufman T, Karpen GH (2006) Drosophila CENP-A mutations cause a BubR1-dependent early mitotic delay without normal localization of kinetochore components. PLoS Genet 2(7):e110.  https://doi.org/10.1371/journal.pgen.0020110CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boden SA, Kavanova M, Finnegan EJ, Wigge PA (2013) Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes. Genome Biol 14(6):R65.  https://doi.org/10.1186/gb-2013-14-6-r65CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cai H, Zhang M, Chai M, He Q, Huang X, Zhao L, Qin Y (2018) Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3. New Phytol.  https://doi.org/10.1111/nph.15306CrossRefGoogle Scholar
  11. Carter B, Bishop B, Ho KK, Huang R, Jia W, Zhang H, Pascuzzi PE, Deal RB, Ogas J (2018) The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis. Plant Cell 30(6):1337–1352.  https://doi.org/10.1105/tpc.17.00867CrossRefPubMedGoogle Scholar
  12. Chaboute ME, Chaubet N, Clement B, Gigot C, Philipps G (1988) Polyadenylation of histone H3 and H4 mRNAs in dicotyledonous plants. Gene 71(1):217–223CrossRefGoogle Scholar
  13. Chaboute ME, Chaubet N, Gigot C, Philipps G (1993) Histones and histone genes in higher plants: structure and genomic organization. Biochimie 75(7):523–531CrossRefGoogle Scholar
  14. Chaubet N, Chaboute ME, Clement B, Ehling M, Philipps G, Gigot C (1988) The histone H3 and H4 mRNAs are polyadenylated in maize. Nucleic Acids Res 16(4):1295–1304CrossRefGoogle Scholar
  15. Chaubet N, Clement B, Gigot C (1992) Genes encoding a histone H3.3-like variant in Arabidopsis contain intervening sequences. J Mol Biol 225(2):569–574CrossRefGoogle Scholar
  16. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, Yelina NE, Hardcastle TJ, Ziolkowski PA, Copenhaver GP, Franklin FC, McVean G, Henderson IR (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45(11):1327–1336.  https://doi.org/10.1038/ng.2766CrossRefPubMedGoogle Scholar
  17. Choi K, Kim J, Muller SY, Oh M, Underwood C, Henderson I, Lee I (2016) Regulation of MicroRNA-mediated developmental changes by the SWR1 chromatin remodeling complex. Plant Physiol 171(2):1128–1143.  https://doi.org/10.1104/pp.16.00332CrossRefPubMedPubMedCentralGoogle Scholar
  18. Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet 8(10):e1002988.  https://doi.org/10.1371/journal.pgen.1002988CrossRefPubMedPubMedCentralGoogle Scholar
  19. Comai L, Maheshwari S, Marimuthu MPA (2017) Plant centromeres. Curr Opin Plant Biol 36:158–167.  https://doi.org/10.1016/j.pbi.2017.03.003CrossRefPubMedGoogle Scholar
  20. Cooper JL, Henikoff S (2004) Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol 21(9):1712–1718.  https://doi.org/10.1093/molbev/msh179CrossRefPubMedGoogle Scholar
  21. Dai X, Bai Y, Zhao L, Dou X, Liu Y, Wang L, Li Y, Li W, Hui Y, Huang X, Wang Z, Qin Y (2017) H2A.Z represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in Arabidopsis. Mol Plant 10(10):1274–1292.  https://doi.org/10.1016/j.molp.2017.09.007CrossRefPubMedGoogle Scholar
  22. De Rop V, Padeganeh A, Maddox PS (2012) CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121(6):527–538.  https://doi.org/10.1007/s00412-012-0386-5CrossRefPubMedPubMedCentralGoogle Scholar
  23. Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19(1):74–83.  https://doi.org/10.1105/tpc.106.048447CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dona M, Mittelsten Scheid O (2015) DNA damage repair in the context of plant chromatin. Plant Physiol 168(4):1206–1218.  https://doi.org/10.1104/pp.15.00538CrossRefPubMedPubMedCentralGoogle Scholar
  25. Eirín-López JM, González-Romero R, Dryhurst D, Méndez J, Ausió J (2009) Long-term evolution of histone families: old notions and new insights into their mechanisms of diversification across eukaryotes. In: Pontarotti P (ed) Evolutionary biology: concept, modeling, and application. Springer, Berlin, pp 139–162.  https://doi.org/10.1007/978-3-642-00952-5_8CrossRefGoogle Scholar
  26. Evtushenko EV, Elisafenko EA, Gatzkaya SS, Lipikhina YA, Houben A, Vershinin AV (2017) Conserved molecular structure of the centromeric histone CENH3 in Secale and its phylogenetic relationships. Sci Rep 7(1):17628.  https://doi.org/10.1038/s41598-017-17932-8CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fabry S, Muller K, Lindauer A, Park PB, Cornelius T, Schmitt R (1995) The organization structure and regulatory elements of Chlamydomonas histone genes reveal features linking plant and animal genes. Curr Genet 28(4):333–345CrossRefGoogle Scholar
  28. Fang Y, Spector DL (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16(12):5710–5718.  https://doi.org/10.1091/mbc.e05-08-0706CrossRefPubMedPubMedCentralGoogle Scholar
  29. Finseth FR, Dong Y, Saunders A, Fishman L (2015) Duplication and adaptive evolution of a key centromeric protein in Mimulus, a genus with female meiotic drive. Mol Biol Evol 32(10):2694–2706.  https://doi.org/10.1093/molbev/msv145CrossRefPubMedGoogle Scholar
  30. Friesner JD, Liu B, Culligan K, Britt AB (2005) Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Mol Biol Cell 16(5):2566–2576.  https://doi.org/10.1091/mbc.e04-10-0890CrossRefPubMedPubMedCentralGoogle Scholar
  31. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102.  https://doi.org/10.1126/science.1062939CrossRefGoogle Scholar
  32. Hereford L, Fahrner K, Woolford J Jr, Rosbash M, Kaback DB (1979) Isolation of yeast histone genes H2A and H2B. Cell 18(4):1261–1271CrossRefGoogle Scholar
  33. Hirsch CD, Wu Y, Yan H, Jiang J (2009) Lineage-specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol Biol Evol 26(12):2877–2885.  https://doi.org/10.1093/molbev/msp208CrossRefPubMedGoogle Scholar
  34. Hoffmann RD, Palmgren MG (2013) Epigenetic repression of male gametophyte-specific genes in the Arabidopsis sporophyte. Mol Plant 6(4):1176–1186.  https://doi.org/10.1093/mp/sst100CrossRefPubMedGoogle Scholar
  35. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, Choo KH (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci U S A 97(3):1148–1153CrossRefGoogle Scholar
  36. Hu Y, Lai Y (2015) Identification and expression analysis of rice histone genes. Plant Physiol Biochem 86:55–65.  https://doi.org/10.1016/j.plaphy.2014.11.012CrossRefGoogle Scholar
  37. Hu Y, Shen Y, Conde ESN, Zhou DX (2011) The role of histone methylation and H2A.Z occupancy during rapid activation of ethylene responsive genes. PLoS One 6(11):e28224.  https://doi.org/10.1371/journal.pone.0028224CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ingouff M, Berger F (2010) Histone3 variants in plants. Chromosoma 119(1):27–33.  https://doi.org/10.1007/s00412-009-0237-1CrossRefGoogle Scholar
  39. Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17(12):1032–1037.  https://doi.org/10.1016/j.cub.2007.05.019CrossRefGoogle Scholar
  40. Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20(23):2137–2143.  https://doi.org/10.1016/j.cub.2010.11.012CrossRefGoogle Scholar
  41. Ishii T, Karimi-Ashtiyani R, Banaei-Moghaddam AM, Schubert V, Fuchs J, Houben A (2015) The differential loading of two barley CENH3 variants into distinct centromeric substructures is cell type- and development-specific. Chromosome Res 23(2):277–284.  https://doi.org/10.1007/s10577-015-9466-8CrossRefPubMedGoogle Scholar
  42. Iwata A, Tek AL, Richard MM, Abernathy B, Fonseca A, Schmutz J, Chen NW, Thareau V, Magdelenat G, Li Y, Murata M, Pedrosa-Harand A, Geffroy V, Nagaki K, Jackson SA (2013) Identification and characterization of functional centromeres of the common bean. Plant J 76(1):47–60.  https://doi.org/10.1111/tpj.12269CrossRefPubMedGoogle Scholar
  43. Jacob Y, Bergamin E, Donoghue MT, Mongeon V, LeBlanc C, Voigt P, Underwood CJ, Brunzelle JS, Michaels SD, Reinberg D, Couture JF, Martienssen RA (2014) Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343(6176):1249–1253.  https://doi.org/10.1126/science.1248357CrossRefPubMedPubMedCentralGoogle Scholar
  44. Jarillo JA, Pineiro M (2015) H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J 83(1):96–109.  https://doi.org/10.1111/tpj.12873CrossRefPubMedGoogle Scholar
  45. Jiang D, Berger F (2017) Histone variants in plant transcriptional regulation. Biochim Biophys Acta Gene Regul Mech 1860(1):123–130.  https://doi.org/10.1016/j.bbagrm.2016.07.002CrossRefGoogle Scholar
  46. Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32(22):6511–6518.  https://doi.org/10.1093/nar/gkh992CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kapros T, Robertson AJ, Waterborg JH (1995) Histone H3 transcript stability in alfalfa. Plant Mol Biol 28(5):901–914CrossRefGoogle Scholar
  48. Karimi-Ashtiyani R, Ishii T, Niessen M, Stein N, Heckmann S, Gurushidze M, Banaei-Moghaddam AM, Fuchs J, Schubert V, Koch K, Weiss O, Demidov D, Schmidt K, Kumlehn J, Houben A (2015) Point mutation impairs centromeric CENH3 loading and induces haploid plants. Proc Natl Acad Sci U S A 112(36):11211–11216.  https://doi.org/10.1073/pnas.1504333112CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kawabe A, Nasuda S, Charlesworth D (2006) Duplication of centromeric histone H3 (HTR12) gene in Arabidopsis halleri and A. lyrata, plant species with multiple centromeric satellite sequences. Genetics 174(4):2021–2032.  https://doi.org/10.1534/genetics.106.063628CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kawashima T, Lorkovic ZJ, Nishihama R, Ishizaki K, Axelsson E, Yelagandula R, Kohchi T, Berger F (2015) Diversification of histone H2A variants during plant evolution. Trends Plant Sci 20(7):419–425.  https://doi.org/10.1016/j.tplants.2015.04.005CrossRefPubMedGoogle Scholar
  51. Kelliher T, Starr D, Wang W, McCuiston J, Zhong H, Nuccio ML, Martin B (2016) Maternal haploids are preferentially induced by CENH3-tailswap transgenic complementation in maize. Front Plant Sci 7:414.  https://doi.org/10.3389/fpls.2016.00414CrossRefPubMedPubMedCentralGoogle Scholar
  52. Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693–705.  https://doi.org/10.1016/j.cell.2007.02.005CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054CrossRefPubMedGoogle Scholar
  54. Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140(1):136–147.  https://doi.org/10.1016/j.cell.2009.11.006CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kuppu S, Tan EH, Nguyen H, Rodgers A, Comai L, Chan SW, Britt AB (2015) Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance. PLoS Genet 11(9):e1005494.  https://doi.org/10.1371/journal.pgen.1005494CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lang J, Smetana O, Sanchez-Calderon L, Lincker F, Genestier J, Schmit AC, Houlne G, Chaboute ME (2012) Plant gammaH2AX foci are required for proper DNA DSB repair responses and colocalize with E2F factors. New Phytol 194(2):353–363.  https://doi.org/10.1111/j.1469-8137.2012.04062.xCrossRefPubMedGoogle Scholar
  57. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948.  https://doi.org/10.1093/bioinformatics/btm404CrossRefGoogle Scholar
  58. Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I (2006) Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18(10):2443–2451.  https://doi.org/10.1105/tpc.106.043174CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, Koszegi D, Schubert I (2011) Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J 68(1):40–50.  https://doi.org/10.1111/j.1365-313X.2011.04664.xCrossRefPubMedGoogle Scholar
  60. Lermontova I, Sandmann M, Mascher M, Schmit AC, Chaboute ME (2015) Centromeric chromatin and its dynamics in plants. Plant J 83(1):4–17.  https://doi.org/10.1111/tpj.12875CrossRefPubMedGoogle Scholar
  61. Li C, Liu Y, Shen WH, Yu Y, Dong A (2018a) Chromatin-remodeling factor OsINO80 is involved in regulation of gibberellin biosynthesis and is crucial for rice plant growth and development. J Integr Plant Biol 60(2):144–159.  https://doi.org/10.1111/jipb.12603CrossRefPubMedGoogle Scholar
  62. Li XR, Deb J, Kumar SV, Ostergaard L (2018b) Temperature modulates tissue-specification program to control fruit Dehiscence in Brassicaceae. Mol Plant 11(4):598–606.  https://doi.org/10.1016/j.molp.2018.01.003CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lorkovic ZJ, Berger F (2017) Heterochromatin and DNA damage repair: use different histone variants and relax. Nucleus 8(6):583–588.  https://doi.org/10.1080/19491034.2017.1384893CrossRefPubMedPubMedCentralGoogle Scholar
  64. Lorkovic ZJ, Park C, Goiser M, Jiang D, Kurzbauer MT, Schlogelhofer P, Berger F (2017) Compartmentalization of DNA damage response between heterochromatin and euchromatin is mediated by distinct H2A histone variants. Curr Biol 27(8):1192–1199.  https://doi.org/10.1016/j.cub.2017.03.002CrossRefPubMedGoogle Scholar
  65. Luger K (2003) Structure and dynamic behavior of nucleosomes. Curr Opin Genet Dev 13(2):127–135CrossRefGoogle Scholar
  66. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389(6648):251–260.  https://doi.org/10.1038/38444CrossRefPubMedPubMedCentralGoogle Scholar
  67. Malik HS, Henikoff S (2001) Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157(3):1293–1298PubMedPubMedCentralGoogle Scholar
  68. Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10(11):882–891.  https://doi.org/10.1038/nsb996CrossRefPubMedPubMedCentralGoogle Scholar
  69. March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio FJ, Reyes JC (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53(3):475–487.  https://doi.org/10.1111/j.1365-313X.2007.03361.xCrossRefPubMedGoogle Scholar
  70. Margueron R, Reinberg D (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11(4):285–296.  https://doi.org/10.1038/nrg2752CrossRefPubMedPubMedCentralGoogle Scholar
  71. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80(5):487–498CrossRefGoogle Scholar
  72. Marzluff WF, Sakallah S, Kelkar H (2006) The sea urchin histone gene complement. Dev Biol 300(1):308–320.  https://doi.org/10.1016/j.ydbio.2006.08.067CrossRefPubMedGoogle Scholar
  73. Masonbrink RE, Gallagher JP, Jareczek JJ, Renny-Byfield S, Grover CE, Gong L, Wendel JF (2014) CenH3 evolution in diploids and polyploids of three angiosperm genera. BMC Plant Biol 14:383.  https://doi.org/10.1186/s12870-014-0383-3CrossRefPubMedPubMedCentralGoogle Scholar
  74. Matsumoto S, Yanagida M (1985) Histone gene organization of fission yeast: a common upstream sequence. EMBO J 4(13A):3531–3538CrossRefGoogle Scholar
  75. Menges M, Hennig L, Gruissem W, Murray JA (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53(4):423–442.  https://doi.org/10.1023/B:PLAN.0000019059.56489.caCrossRefPubMedGoogle Scholar
  76. Montellier E, Boussouar F, Rousseaux S, Zhang K, Buchou T, Fenaille F, Shiota H, Debernardi A, Hery P, Curtet S, Jamshidikia M, Barral S, Holota H, Bergon A, Lopez F, Guardiola P, Pernet K, Imbert J, Petosa C, Tan M, Zhao Y, Gerard M, Khochbin S (2013) Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev 27(15):1680–1692.  https://doi.org/10.1101/gad.220095.113CrossRefPubMedPubMedCentralGoogle Scholar
  77. Moraes I, Yuan ZF, Liu S, Souza GM, Garcia BA, Casas-Mollano JA (2015) Analysis of histones H3 and H4 reveals novel and conserved post-translational modifications in sugarcane. PLoS One 10(7):e0134586.  https://doi.org/10.1371/journal.pone.0134586CrossRefPubMedPubMedCentralGoogle Scholar
  78. Moraes IC, Lermontova I, Schubert I (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol Biol 75(3):253–261.  https://doi.org/10.1007/s11103-010-9723-3CrossRefPubMedGoogle Scholar
  79. Muller K, Schmitt R (1988) Histone genes of Volvox carteri: DNA sequence and organization of two H3-H4 gene loci. Nucleic Acids Res 16(9):4121–4136CrossRefGoogle Scholar
  80. Muller K, Lindauer A, Bruderlein M, Schmitt R (1990) Organization and transcription of Volvox histone-encoding genes: similarities between algal and animal genes. Gene 93(2):167–175CrossRefGoogle Scholar
  81. Mysore KS, Nam J, Gelvin SB (2000) An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. Proc Natl Acad Sci U S A 97(2):948–953CrossRefGoogle Scholar
  82. Nagaki K, Murata M (2005) Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13(2):195–203.  https://doi.org/10.1007/s10577-005-0847-2CrossRefPubMedGoogle Scholar
  83. Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J (2003) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163(3):1221–1225PubMedPubMedCentralGoogle Scholar
  84. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36(2):138–145.  https://doi.org/10.1038/ng1289CrossRefPubMedGoogle Scholar
  85. Nagaki K, Kashihara K, Murata M (2009) A centromeric DNA sequence colocalized with a centromere-specific histone H3 in tobacco. Chromosoma 118(2):249–257.  https://doi.org/10.1007/s00412-008-0193-1CrossRefPubMedGoogle Scholar
  86. Neumann P, Pavlikova Z, Koblizkova A, Fukova I, Jedlickova V, Novak P, Macas J (2015) Centromeres off the hook: massive changes in centromere size and structure following duplication of CenH3 gene in Fabeae species. Mol Biol Evol 32(7):1862–1879.  https://doi.org/10.1093/molbev/msv070CrossRefPubMedPubMedCentralGoogle Scholar
  87. Okada T, Endo M, Singh MB, Bhalla PL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44(4):557–568.  https://doi.org/10.1111/j.1365-313X.2005.02554.xCrossRefGoogle Scholar
  88. Okada T, Singh MB, Bhalla PL (2006) Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol Biol 62(4-5):503–512.  https://doi.org/10.1007/s11103-006-9036-8CrossRefGoogle Scholar
  89. Osakabe A, Lorkovic ZJ, Kobayashi W, Tachiwana H, Yelagandula R, Kurumizaka H, Berger F (2018) Histone H2A variants confer specific properties to nucleosomes and impact on chromatin accessibility. Nucleic Acids Res 46(15):7675–7685.  https://doi.org/10.1093/nar/gky540CrossRefPubMedPubMedCentralGoogle Scholar
  90. Postberg J, Forcob S, Chang WJ, Lipps HJ (2010) The evolutionary history of histone H3 suggests a deep eukaryotic root of chromatin modifying mechanisms. BMC Evol Biol 10:259.  https://doi.org/10.1186/1471-2148-10-259CrossRefPubMedPubMedCentralGoogle Scholar
  91. Qin Y, Zhao L, Skaggs MI, Andreuzza S, Tsukamoto T, Panoli A, Wallace KN, Smith S, Siddiqi I, Yang Z, Yadegari R, Palanivelu R (2014) ACTIN-RELATED PROTEIN6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. Plant Cell 26(4):1612–1628.  https://doi.org/10.1105/tpc.113.120576CrossRefPubMedPubMedCentralGoogle Scholar
  92. Rattray AM, Muller B (2012) The control of histone gene expression. Biochem Soc Trans 40(4):880–885.  https://doi.org/10.1042/BST20120065CrossRefPubMedGoogle Scholar
  93. Ravi M, Chan SW (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464(7288):615–618.  https://doi.org/10.1038/nature08842CrossRefGoogle Scholar
  94. Ravi M, Kwong PN, Menorca RM, Valencia JT, Ramahi JS, Stewart JL, Tran RK, Sundaresan V, Comai L, Chan SW (2010) The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics 186(2):461–471.  https://doi.org/10.1534/genetics.110.120337CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen C, Murata M, Chan SW (2011) Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PLoS Genet 7(6):e1002121.  https://doi.org/10.1371/journal.pgen.1002121CrossRefPubMedPubMedCentralGoogle Scholar
  96. Reichheld JP, Gigot C, Chaubet-Gigot N (1998) Multilevel regulation of histone gene expression during the cell cycle in tobacco cells. Nucleic Acids Res 26(13):3255–3262CrossRefGoogle Scholar
  97. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273(10):5858–5868CrossRefGoogle Scholar
  98. Roitinger E, Hofer M, Kocher T, Pichler P, Novatchkova M, Yang J, Schlogelhofer P, Mechtler K (2015) Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol Cell Proteomics 14(3):556–571.  https://doi.org/10.1074/mcp.M114.040352CrossRefPubMedPubMedCentralGoogle Scholar
  99. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A (2011) Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci U S A 108(33):E498–E505.  https://doi.org/10.1073/pnas.1103190108CrossRefPubMedPubMedCentralGoogle Scholar
  100. Santoro SW, Dulac C (2012) The activity-dependent histone variant H2BE modulates the life span of olfactory neurons. Elife 1:e00070.  https://doi.org/10.7554/eLife.00070CrossRefPubMedPubMedCentralGoogle Scholar
  101. Shi L, Wang J, Hong F, Spector DL, Fang Y (2011) Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. Proc Natl Acad Sci U S A 108(26):10574–10578.  https://doi.org/10.1073/pnas.1017882108CrossRefPubMedPubMedCentralGoogle Scholar
  102. Shu H, Nakamura M, Siretskiy A, Borghi L, Moraes I, Wildhaber T, Gruissem W, Hennig L (2014) Arabidopsis replacement histone variant H3.3 occupies promoters of regulated genes. Genome Biol 15(4):R62.  https://doi.org/10.1186/gb-2014-15-4-r62CrossRefPubMedPubMedCentralGoogle Scholar
  103. Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, Meagher RB (2010) Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol 152(1):217–225.  https://doi.org/10.1104/pp.109.145532CrossRefPubMedPubMedCentralGoogle Scholar
  104. Smith MM, Andresson OS (1983) DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol 169(3):663–690CrossRefGoogle Scholar
  105. Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci U S A 109(14):5370–5375.  https://doi.org/10.1073/pnas.1203145109CrossRefPubMedPubMedCentralGoogle Scholar
  106. Sura W, Kabza M, Karlowski WM, Bieluszewski T, Kus-Slowinska M, Paweloszek L, Sadowski J, Ziolkowski PA (2017) Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 29(4):791–807.  https://doi.org/10.1105/tpc.16.00573CrossRefPubMedPubMedCentralGoogle Scholar
  107. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3(2):137–144.  https://doi.org/10.1038/nrg733CrossRefGoogle Scholar
  108. Tabata T, Iwabuchi M (1984) Molecular cloning and nucleotide sequence of a variant wheat histone H4 gene. Gene 31(1-3):285–289CrossRefGoogle Scholar
  109. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14(5):1053–1066CrossRefGoogle Scholar
  110. Talbert PB, Bryson TD, Henikoff S (2004) Adaptive evolution of centromere proteins in plants and animals. J Biol 3(4):18.  https://doi.org/10.1186/jbiol11CrossRefPubMedPubMedCentralGoogle Scholar
  111. Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SW, Cross GA, Cui L, Dimitrov SI, Doenecke D, Eirin-Lopez JM, Gorovsky MA, Hake SB, Hamkalo BA, Holec S, Jacobsen SE, Kamieniarz K, Khochbin S, Ladurner AG, Landsman D, Latham JA, Loppin B, Malik HS, Marzluff WF, Pehrson JR, Postberg J, Schneider R, Singh MB, Smith MM, Thompson E, Torres-Padilla ME, Tremethick DJ, Turner BM, Waterborg JH, Wollmann H, Yelagandula R, Zhu B, Henikoff S (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5:7.  https://doi.org/10.1186/1756-8935-5-7CrossRefPubMedPubMedCentralGoogle Scholar
  112. Tek AL, Kashihara K, Murata M, Nagaki K (2011) Functional centromeres in Astragalus sinicus include a compact centromere-specific histone H3 and a 20-bp tandem repeat. Chromosome Res 19(8):969–978.  https://doi.org/10.1007/s10577-011-9247-yCrossRefPubMedGoogle Scholar
  113. Tenea GN, Spantzel J, Lee LY, Zhu Y, Lin K, Johnson SJ, Gelvin SB (2009) Overexpression of several Arabidopsis histone genes increases agrobacterium-mediated transformation and transgene expression in plants. Plant Cell 21(10):3350–3367.  https://doi.org/10.1105/tpc.109.070607CrossRefPubMedPubMedCentralGoogle Scholar
  114. Ueda K, Kinoshita Y, Xu ZJ, Ide N, Ono M, Akahori Y, Tanaka I, Inoue M (2000) Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum. Chromosoma 108(8):491–500CrossRefGoogle Scholar
  115. Ueda K, Suzuki M, Ono M, Ide N, Tanaka I, 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(2):229–238.  https://doi.org/10.1007/s11103-005-8521-9CrossRefPubMedGoogle Scholar
  116. Wang G, He Q, Liu F, Cheng Z, Talbert PB, Jin W (2011) Characterization of CENH3 proteins and centromere-associated DNA sequences in diploid and allotetraploid Brassica species. Chromosoma 120(4):353–365.  https://doi.org/10.1007/s00412-011-0315-zCrossRefPubMedGoogle Scholar
  117. Waterborg JH (1990) Sequence analysis of acetylation and methylation in two histone H3 variants of alfalfa. J Biol Chem 265(28):17157–17161PubMedGoogle Scholar
  118. Waterborg JH (1991) Multiplicity of histone h3 variants in wheat, barley, rice, and maize. Plant Physiol 96(2):453–458CrossRefGoogle Scholar
  119. Waterborg JH (2012) Evolution of histone H3: emergence of variants and conservation of post-translational modification sites. Biochem Cell Biol 90(1):79–95.  https://doi.org/10.1139/o11-036CrossRefPubMedGoogle Scholar
  120. Waterborg JH, Robertson AJ (1996) Common features of analogous replacement histone H3 genes in animals and plants. J Mol Evol 43(3):194–206CrossRefGoogle Scholar
  121. Wollmann H, Holec S, Alden K, Clarke ND, Jacques PE, Berger F (2012) Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLoS Genet 8(5):e1002658.  https://doi.org/10.1371/journal.pgen.1002658CrossRefPubMedPubMedCentralGoogle Scholar
  122. Wollmann H, Stroud H, Yelagandula R, Tarutani Y, Jiang D, Jing L, Jamge B, Takeuchi H, Holec S, Nie X, Kakutani T, Jacobsen SE, Berger F (2017) The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana. Genome Biol 18(1):94.  https://doi.org/10.1186/s13059-017-1221-3CrossRefPubMedPubMedCentralGoogle Scholar
  123. Wu SC, Gyorgyey J, Dudits D (1989) Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucleic Acids Res 17(8):3057–3063CrossRefGoogle Scholar
  124. Wu T, Yuan T, Tsai SN, Wang C, Sun SM, Lam HM, Ngai SM (2009) Mass spectrometry analysis of the variants of histone H3 and H4 of soybean and their post-translational modifications. BMC Plant Biol 9:98.  https://doi.org/10.1186/1471-2229-9-98CrossRefPubMedPubMedCentralGoogle Scholar
  125. Xu H, Swoboda I, Bhalla PL, Singh MB (1999) Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol Biol 39(3):607–614CrossRefGoogle Scholar
  126. Xu M, Leichty AR, Hu T, Poethig RS (2018) H2A.Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3. Development 145(2).  https://doi.org/10.1242/dev.152868CrossRefGoogle Scholar
  127. Yang H, Yang N, Wang T (2016) Proteomic analysis reveals the differential histone programs between male germline cells and vegetative cells in Lilium davidii. Plant J 85(5):660–674.  https://doi.org/10.1111/tpj.13133CrossRefGoogle Scholar
  128. Yelagandula R, Stroud H, Holec S, Zhou K, Feng S, Zhong X, Muthurajan UM, Nie X, Kawashima T, Groth M, Luger K, Jacobsen SE, Berger F (2014) The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158(1):98–109.  https://doi.org/10.1016/j.cell.2014.06.006CrossRefPubMedPubMedCentralGoogle Scholar
  129. Yi H, Sardesai N, Fujinuma T, Chan CW, Veena, Gelvin SB (2006) Constitutive expression exposes functional redundancy between the Arabidopsis histone H2A gene HTA1 and other H2A gene family members. Plant Cell 18(7):1575–1589.  https://doi.org/10.1105/tpc.105.039719CrossRefPubMedPubMedCentralGoogle Scholar
  130. Yu N, Nutzmann HW, MacDonald JT, Moore B, Field B, Berriri S, Trick M, Rosser SJ, Kumar SV, Freemont PS, Osbourn A (2016) Delineation of metabolic gene clusters in plant genomes by chromatin signatures. Nucleic Acids Res 44(5):2255–2265.  https://doi.org/10.1093/nar/gkw100CrossRefPubMedPubMedCentralGoogle Scholar
  131. Yuan J, Guo X, Hu J, Lv Z, Han F (2015) Characterization of two CENH3 genes and their roles in wheat evolution. New Phytol 206(2):839–851.  https://doi.org/10.1111/nph.13235CrossRefPubMedGoogle Scholar
  132. Zahraeifard S, Foroozani M, Sepehri A, Oh DH, Wang G, Mangu V, Chen B, Baisakh N, Dassanayake M, Smith AP (2018) Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes. J Exp Bot 69(20):4907–4919.  https://doi.org/10.1093/jxb/ery244CrossRefPubMedPubMedCentralGoogle Scholar
  133. Zedek F, Bures P (2016a) Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Ann Bot 118(7):1347–1352.  https://doi.org/10.1093/aob/mcw186CrossRefPubMedPubMedCentralGoogle Scholar
  134. Zedek F, Bures P (2016b) CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model. Sci Rep 6:33308.  https://doi.org/10.1038/srep33308CrossRefPubMedPubMedCentralGoogle Scholar
  135. Zhang K, Xu W, Wang C, Yi X, Su Z (2017a) Differential deposition of H2A.Z in rice seedling tissue during the day-night cycle. Plant Signal Behav 12(3):e1286438.  https://doi.org/10.1080/15592324.2017.1286438CrossRefPubMedPubMedCentralGoogle Scholar
  136. Zhang K, Xu W, Wang C, Yi X, Zhang W, Su Z (2017b) Differential deposition of H2A.Z in combination with histone modifications within related genes in Oryza sativa callus and seedling. Plant J 89(2):264–277.  https://doi.org/10.1111/tpj.13381CrossRefPubMedGoogle Scholar
  137. Zheng YE, He XW, Ying YH, Lu JF, Gelvin SB, Shou HX (2009) Expression of the Arabidopsis thaliana histone gene AtHTA1 enhances rice transformation efficiency. Mol Plant 2(4):832–837.  https://doi.org/10.1093/mp/ssp038CrossRefPubMedGoogle Scholar
  138. Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang J, Dawe RK (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14(11):2825–2836CrossRefGoogle Scholar
  139. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456(7218):125–129.  https://doi.org/10.1038/nature07324CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Marlon S. Zambrano-Mila
    • 1
  • Maria J. Aldaz-Villao
    • 1
  • Juan Armando Casas-Mollano
    • 1
  1. 1.School of Biological Sciences and EngineeringYachay Tech UniversitySan Miguel de UrcuquíEcuador

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