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Common features of analogous replacement histone H3 genes in animals and plants

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Abstract

Phylogenetic analysis of histone H3 protein sequences demonstrates the independent origin of the replacement histone H3 genes in animals and in plants. Multiple introns in the replacement histone H3 genes of animals in a pattern distinct from that in plant replacement H3 genes supports this conclusion. It is suggested that replacement H3 genes arose at the same time that, independently, multicellular forms of animals and of plants evolved. Judged by the degree of invariant and functionally constrained amino acid positions, histones H3 and H4, which form together the tetramer kernel of the nucleosome, have co-evolved with equal rates of sequence divergence. Residues 31 and 87 in histone H3 are the only residues that consistently changed across each gene duplication event that created functional replacement histone H3 variant forms. Once changed, these residues have remained invariant across divergent speciation. This suggests that they are required to allow replacement histone H3 to participate in the assembly of nucleosomes in non-S-phase cells. The abundant occurrence of polypyrimidine sequences in the introns of all replacement H3 genes, and the replacement of an intron by a polypyrimidine motif upstream of the alfalfa replacement H3 gene, suggests a function. It is speculated that they may contribute to the characteristic cell-cycle-independent pattern of replacement histone H3 genes by binding nucleosome-excluding proteins.

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References

  • Arents G, Moudrianakis EN (1993) Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci USA 90:10489–10493.

    CAS  PubMed  Google Scholar 

  • Arents G, Moudrianakis EN (1995) The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci USA 92:11170–11174

    CAS  PubMed  Google Scholar 

  • Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN (1991) The nucleosomal core histone octamer at 3.1 Å resolution. A tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci USA 88:10138–10148

    Google Scholar 

  • Bannon GA, Calzone FJ, BowenJK, Allis CD, Gorovsky MA (1983) Multiple, independently regulated, polyadenylated messages for histone H3 and H4 in Tetrahymena. Nucleic Acids Res 11:3903–3917

    CAS  PubMed  Google Scholar 

  • Baxevanis AD, Landsman D (1996) Histone sequence database: a compilation of highly-conserved nucleoprotein sequences. Nucleic Acids Res 24:245–247

    Article  CAS  PubMed  Google Scholar 

  • Biggin MD, Tjian R (1988) Transcription factors that activate the ultrabithorax promoter in developmentally staged extracts. Cell 53: 699–711

    CAS  PubMed  Google Scholar 

  • Björkroth B, Ericsson C, Lamb MM, Daneholt B (1988) Structure of the chromatin axis during transcription. Chromosoma 96:333–340

    Article  Google Scholar 

  • Brocard MP, Rousseau D, Lawrence JJ, Khochbin S (1994) Two mRNA species encoding the differentiation-associated histone H1° are produced by alternative polyadenylation in mouse. Eur J Biochem 221:421–425

    Article  CAS  PubMed  Google Scholar 

  • Chaboute ME, Chaubet N, Clement B, Gigot C, Philipps G (1988) Polyadenylation of histone H3 and H4 mRNAs in dicotyledonous plants. Gene 71:217–223

    Article  CAS  PubMed  Google Scholar 

  • Chaboute ME, Chaubet N, Gigot C, Philipps G (1993) Histories and histone genes in higher plants: structure and genomic organization. Biochimie 75:523–531

    Article  CAS  PubMed  Google Scholar 

  • Chaubet N, Chaboute ME, Clement B, Ehling M, Philipps G, Gigot C (1988) The histone H3 and H4 messenger RNAs are polyadenylated in maize. Nucleic Acids Res 16:1295–1304

    CAS  PubMed  Google Scholar 

  • Chaubet N, Clement B, Gigot C (1992) Genes encoding a histone H3.3-like variant in Arabidopsis contain intervening sequences. J Mol Biol 225:569–574

    Article  CAS  PubMed  Google Scholar 

  • Desjardins E, Hay N (1993) Repeated CT elements bound by zinc-finger proteins control the absolute and relative activities of the two principal human c-myc promoters. Mol Cell Biol 13:5710–5724

    CAS  PubMed  Google Scholar 

  • Fabry S, Müller 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 28:333–345

    Article  CAS  PubMed  Google Scholar 

  • Fahmer K, Yarger J, Hereford L (1980) Yeast histone mRNA is polyadenylated. Nucleic Acids Res 8:5725–5737

    Google Scholar 

  • Fodinger M, Ortner S, Plaimauer B, Wiedermann G, Scheiner O, Duchene M (1993) Pathogenic Entamoeba histolytica: cDNA cloning of a histone H3 with a divergent primary structure. Mol Biochem Parasitol 59:315–322

    Article  CAS  PubMed  Google Scholar 

  • Heintz N (1991) The regulation of histone gene expression during the cell cycle. Biochim Biophys Acta 1088:327–340

    CAS  PubMed  Google Scholar 

  • Hillis DM, Huelsenbeck JP, Cunningham CW (1994) Application and accuracy of molecular phylogenies. Science 264:671–677

    CAS  PubMed  Google Scholar 

  • Kapros T, Bögre L, Németh K, Bakó L, Györgyey J, Wu S-C, Dudits D (1992) Differential expression of histone H3 gene variants during cell cycle and somatic embryogenesis in alfalfa. Plant Physiol 98: 621–625

    CAS  Google Scholar 

  • Kapros T, Robertson AJ, Waterborg JH (1995) Histone H3 transcript stability in alfalfa. Plant Mol Biol 28:901–914

    Article  CAS  PubMed  Google Scholar 

  • Kirsh AL, Groudine M, Challoner PB (1989) Polyadenylation and U7 snRNP-mediated cleavage—alternative modes of RNA 3' processing in two avian histone Hl genes. Genes Dev 3:2172–2179

    CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (1993) MEGA: Molecular Evolutionary Genetics Analysis, version 1.0. The Pennsylvania University,University Park, PA

    Google Scholar 

  • Laner M, de Bruin D, Wertheimer SP, Ravetch JV (1994) Transcriptional and nucleosomal characterization of a subtelomeric gene cluster flanking a site of chromosomal rearrangements in Plasmodium falciparum. Nucleic Acids Res 22:4176–4182

    Google Scholar 

  • Li B, Adams CC, Workman JL (1994) Nucleosome binding by the constitutive transcription factor Spl. J Biol Chem 269: 7756–7763

    CAS  PubMed  Google Scholar 

  • Lu Q, Wallrath LL, Granok H, Elgin SC (1993) (CT)n (GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol Cell Biol 13:2802–2814

    CAS  PubMed  Google Scholar 

  • Mannironi C, Bonner WM, Hatch CL (1989) H2A.X, a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3′ processing signals. Nucleic Acids Res 17:9113–9126

    CAS  PubMed  Google Scholar 

  • Marzluff WF (1989) Histone gene expression not coupled to DNA synthesis. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic proteins. CRC Press, Boca Raton, FL

    Google Scholar 

  • Marzluff WF (1992) Histone 3' ends: essential and regulatory functions. Gene Expr 2:93–97

    CAS  PubMed  Google Scholar 

  • Matthews HR, Waterborg JH (1985) Reversible modifications of nuclear proteins and their significance. In: Freedman RB, Hawkins HC (eds) The enzymology of post-translational modification of proteins, vol 2. Academic Press, London

    Google Scholar 

  • Michalon P, Couturier R, Bender K, Hecker H, Marion C (1993) Structural analysis of Trypanosoma brucei brucei chromatin by limited proteolysis. An electrical birefringence study. Eur J Biochem 216: 387–394

    Article  CAS  PubMed  Google Scholar 

  • Muller SB, Reusing SA, Maier UG (1994) The cryptomonas histone H4-encoding gene: structure and chromosomal location. Gene 150: 299–302

    CAS  PubMed  Google Scholar 

  • O'Brien T, Wilkins RC, Giardina C, Lis JT (1995) Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev 9:1098–1110

    PubMed  Google Scholar 

  • O'Donnell KH, Wensink PC (1994) GAGA factor and TBF1 bind DNA elements that direct ubiquitous transcription of the α1-tubulin gene. Nucleic Acids Res 22:4712–4718

    PubMed  Google Scholar 

  • O'Donnell KH, Chen CT, Wensink P (1994) Insulating DNA directs ubiquitous transcription of the Drosophila melanogaster αl-tubulin gene. Mol Cell Biol 14:6398–6408

    PubMed  Google Scholar 

  • Old RW, Woodland HR (1984) Histone genes: not so simple after all. Cell 38:624–626

    Article  CAS  PubMed  Google Scholar 

  • Osley MA (1991) The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60:827–861

    Article  CAS  PubMed  Google Scholar 

  • Peltz SW, Brewer G, Bernstein P, Hart PA, Ross J (1991) Regulation of mRNA turnover in eukaryryotec cells. Crit Rev Eukaryot Gene Expr 1:99–126

    CAS  PubMed  Google Scholar 

  • Puerta C, Martin J, Alonso C, Lopez MC (1994) Isolation and characterization of the gene encoding histone H2A from Trypanosoma cruzi. Mol Biochem Parasitol 64:1–10

    Article  CAS  PubMed  Google Scholar 

  • Robertson AJ, Kapros T, Dudits D, Waterborg JH (1995) Identification of the three highly expressed replacement histone H3 genes of alfalfa. DNA Seq (in press)

  • Sadler LA, Brunk CF (1992) Phylogenetic relationships and unusual diversity in histone H4 proteins within the Tetrahymena pyriformis complex. Mol Biol Evol 9:70–84

    CAS  PubMed  Google Scholar 

  • Saint-Guily A, Schantz ML, Schantz R (1994) Structure and expression of a cDNA encoding a histone H2A from Euglena gracilis. Plant Mol Biol 24:941–948

    Article  CAS  PubMed  Google Scholar 

  • Schlimme W, Burri M, Bender K, Betschart B, Hecker H (1993) Trypanosoma brucei brucei: differences in the nuclear chromatin of bloodstream forms and procyclic culture forms. Parasitology 107: 237–247

    PubMed  Google Scholar 

  • Soto M, Requena JM, Jimenez-Ruiz A, Alonso C (1991) The messenger RNA coding for the nucleosomal protein H2A of Leishmania is polyadenylated and has stem-loops at the 3′ end. Nucleic Acids Res 19:4554

    CAS  PubMed  Google Scholar 

  • Soto M, Requena JM, Morales G, Alonso C (1994) The Leishmania infantum histone H3 possesses an extremely divergent N-terminal domain. Biochem Biophys Acta 1219:533–535

    CAS  PubMed  Google Scholar 

  • Standart N, Dale M (1993) Regulated polyadenylation of clam maternal mRNAs in vitro. Dev Genet 14:492–499

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (1993) PAUP: Phylogenetic analysis using parsimony, version 3.1.1. Illinois Natural History Survey, Campaign, IL

    Google Scholar 

  • Thatcher TH, MacGaffey J, Bowen J, Horowitz S, Shapiro DL, Gorovsky MA (1994) Independent evolutionary origin of histone H3.3-like variants of animals and Tetrahymena. Nucleic Acids Res 22: 180–186

    CAS  PubMed  Google Scholar 

  • Tsukiyama T, Becker PB, Wu C (1994) ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367:525–532

    Article  CAS  PubMed  Google Scholar 

  • Urban MK, Zweidler A (1983) Changes in nucleosomal core histone variants during chicken development and maturation. Dev Biol 95: 421–428

    Article  CAS  PubMed  Google Scholar 

  • VanDaal A, White EM, Elgin SC, Gorovsky MA (1990) Conservation of intron position indicates separation of major and variant H2As is an early event in the evolution of eukaryotes. J Mol Evol 30: 449–455

    CAS  Google Scholar 

  • Vanfleteren JR, VanBun SM, VanBeeumen JJ (1989) The histones of Caenorhabditis elegans. No evidence of stage specific isoforms—an overview. FEBS Lett 257:233–237

    Article  CAS  PubMed  Google Scholar 

  • Van Holde KE (1989) Chromatin. In: Chromatin. Springer Verlag, New York

    Google Scholar 

  • Wall G, Varga-Weisz PD, Sandaltzopoulos R, Becker PB (1995) Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. EMBO J 14: 1727–1736

    CAS  PubMed  Google Scholar 

  • Waterborg JH (1990) Sequence analysis of acetylation and methylation of two histone H3 variants of alfalfa. J Biol Chem 265:17157–17161

    CAS  PubMed  Google Scholar 

  • Waterborg JH (1991) Multiplicity of histone H3 variants in wheat, barley, rice and maize. Plant Physiol 96:453–458

    CAS  Google Scholar 

  • Waterborg JH (1992) Existence of two histone H3 variants in dicotyledonous plants and correlation between their acetylation and plant genome size. Plant Mol Biol 18:181–187

    Article  CAS  PubMed  Google Scholar 

  • Waterborg JH (1993) Histone synthesis and turnover in alfalfa. Fast loss of highly acetylated replacement histone H3.2. J Biol Chem 268:4912–4917

    CAS  PubMed  Google Scholar 

  • Waterborg JH, Robertson AJ, Tatar DL, Borza CM, Davie JR (1995) Histones of Chlamydomonas reinhardtii. Synthesis, acetylation and methylation. Plant Physiol 109:393–407

    Article  CAS  PubMed  Google Scholar 

  • Wells JRE, Coles LS, Robins AJ (1989) Organization of histone genes and their variants. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic proteins. CRC Press, Boca Raton, FL

    Google Scholar 

  • Wilhelm ME, Toublan B, Fujita RA, Wilhelm FX (1988) Histone H4 messenger RNA is stored as a small cytoplasmic rnp during the G2 phase in Physarum polycephalum. Biochem Biophys Res Commun 153:162–171

    Article  CAS  PubMed  Google Scholar 

  • Williams AS, Ingledue TC, Kay BK, Marzluff WF (1994) Changes in the stem-loop at the 3′ terminus of histone mRNA affect its nucleoplasmic transport and cytoplasmic regulation. Nucleic Acids Res 22:4660–4666

    CAS  PubMed  Google Scholar 

  • Wu S-C, Györgyey J, Dudits D (1989) Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucleic Acids Res 17:3057–3063

    CAS  PubMed  Google Scholar 

  • Zhong R, Roeder RG, Heintz N (1983) The primary structure and expression of four cloned human histone genes. Nucleic Acids Res 11:7409–7425

    CAS  PubMed  Google Scholar 

  • Zweidler A (1984) Core histone variants of the mouse: primary structure and differential expression. In: Stein GS, Stein JL, Marzluff WF (eds) Histone genes: structure, organization and regulation. John Wiley & Sons, New York

    Google Scholar 

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Correspondence to: J. H. Waterborg

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Waterborg, J.H., Robertson, A.J. Common features of analogous replacement histone H3 genes in animals and plants. J Mol Evol 43, 194–206 (1996). https://doi.org/10.1007/BF02338827

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