Molecular Biology and Evolution 19:689-697 (2002)
© 2002 Society for Molecular Biology and Evolution
Purifying Selection and Birth-and-death Evolution in the Histone H4 Gene Family
Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University
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Abstract |
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Histones are small basic proteins encoded by a multigene family and are responsible for the nucleosomal organization of chromatin in eukaryotes. Because of the high degree of protein sequence conservation, it is generally believed that histone genes are subject to concerted evolution. However, purifying selection can also generate a high degree of sequence homogeneity. In this study, we examined the long-term evolution of histone H4 genes to determine whether concerted evolution or purifying selection was the major factor for maintaining sequence homogeneity. We analyzed the proportion (pS) of synonymous nucleotide differences between the H4 genes from 59 species of fungi, plants, animals, and protists and found that pS is generally very high and often close to the saturation level (pS ranging from 0.3 to 0.6) even though protein sequences are virtually identical for all H4 genes. A small proportion of genes showed a low level of pS values, but this appeared to be caused by recent gene duplication. Our findings suggest that the members of this gene family evolve according to the birth-and-death model of evolution under strong purifying selection. Using histone-like genes in archaebacteria as outgroups, we also showed that H1, H2A, H2B, H3, and H4 histone genes in eukaryotes form separate clusters and that these classes of genes diverged nearly at the same time, before the eukaryotic kingdoms diverged.
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Histones are highly conserved eukaryotic proteins and are responsible for the packaging of chromosomal DNA into nucleosomes (Pereira et al. 1997
; Sandman and Reeve 2000
). The eukaryotic nucleosome contains approximately 200 bp of DNA wrapped around an octamer of four different classes of histones (H2A, H2B, H3, and H4) and is loosely associated with a linker histone (H1). Among prokaryotes, one lineage of archaebacteria, Euryarchaeota, is known to have histone-like proteins. These histone-like proteins also bind and wrap DNA into nucleosomal structures (Bailey et al. 2000
), but their relatively small size and absence of diversification into separate classes clearly distinguishes them from eukaryotic histones (Wu et al. 2000
). In general, histone protein sequences are highly conserved within and between species. However, protists show a moderate amount of protein sequence diversity compared with other eukaryotes (Sadler and Brunk 1992
; Bernhard and Schlegel 1998
). This higher level of histone sequence diversity in protists may be attributed to the fact that they do not have condensed chromatin (e.g., Trypanosoma spp.; Espinoza et al. 1996
), unlike higher eukaryotes (i.e., fungi, plants, and animals).
Among higher eukaryotic species, H4 proteins are highly conserved and show almost identical amino acid sequences within and between species (fig. 1
). Although purifying selection certainly plays an important role in maintaining the high level of H4 protein sequence conservation, the observed amino acid sequence homogeneity is often explained by concerted evolution (Dover 1982
; Maxson et al. 1983
; Taylor, Wellman, and Marzluff 1986
; Matsuo and Yamazaki 1989
; DeBry and Marzluff 1994
; Wang et al. 1996a, 1996b;
Baldo, Les, and Strausbaugh 1999
; Liao 1999
). Concerted evolution can be defined as a process whereby individual members of a gene family do not evolve independently but instead evolve together as a unit by means of gene conversion or unequal crossing-over (Smith 1974
; Arnheim 1983
). In general, concerted evolution is expected to generate a higher degree of sequence similarity among multiple copies of genes within species than between species. However, histone H4 protein sequences are very similar even between distantly related species, such as animals and plants. This suggests that the major force for H4 protein homogeneity is purifying selection at the protein level.
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Nevertheless, concerted evolution may take place at the DNA level. If this is the case, the DNA sequences of different member genes will be very similar within species but different between species. In the presence of strong purifying selection without concerted evolution, DNA sequence differences will be observed primarily at the synonymous sites. In this case, if the member genes evolve independently following the model of birth-and-death evolution as proposed by Nei and Hughes (1992)
, the DNA sequences of different member genes can be very different both within and between species at synonymous sites (Nei, Gu, and Sitnikova 1997
). The birth-and-death model of evolution assumes that new genes are created by repeated gene duplication and that some of the duplicate genes are maintained in the genome for a long time, whereas others are deleted or become nonfunctional (Nei and Hughes 1992
; Ota and Nei 1994
; Nei, Gu, and Sitnikova 1997
). It is possible to distinguish between the hypotheses of concerted evolution and birth-and-death evolution under strong purifying selection by examining the extent of synonymous differences within and between species. If intraspecific synonymous differences were nearly as high as interspecific differences, this would suggest that birth-and-death evolution under strong purifying selection is the dominant force. In this paper we investigate the mode of evolution of the histone H4 gene family by examining the proportion of synonymous (pS) and nonsynonymous (pN) differences per site between histone H4 genes both within and between species. The results obtained are presented subsequently. |
Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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A total of 137 histone H4 gene sequences from 4 protists, 11 plants, 8 fungi, and 36 animal species were obtained from GenBank. The complete genome sequence of Caenorhabditis elegans is now available (C. elegans Sequencing Consortium, 1998
), and we included the entire set of histone H4 gene sequences from this species, i.e., 16 gene sequences. In addition, partial sequence data from the genome of Caenorhabditis briggsae, which is currently being sequenced, are publicly available. We have therefore included five H4 genes sequenced from this species. The numbers of gene sequences used from the other species are presented as follows (gene numbers are shown in brackets). Protists: Giardia (1), Leishmania (3), Phreatamoeba (1), and Pyrenomonas (1). Fungi: Agaricus (1), Aspergillus nidulans (2), Aspergillus oryzae (1), Neurospora (1), Phanerochaete (2), Saccharomyces pastorianus (1), Saccharomyces cerevisiae (4), and Schizosaccharomyces (3). Plants: Chlamydomonas (4), Volvox (1), Arabidopsis (7), Capsicum (1), Lolium (1), Lycopersicon (2), Pisum (1), Sesbania (2), Solanum (1), Triticum (2), and Zea (4). Animals: Acropora (2), Ascaris (1), Chaetopterus (1), Platynereis (1), Urechis (1), Asellus (1), Tigriopus (1), Acrolepiopsis (1), Apis (1), Chironomus (2), Diadromus (1), Diprion (1), Drosophila hydei (3), Drosophila melanogaster (2), Trichogramma (1), Holothuria (1), Lytechinus (2), Paracentrotus (2), Pisaster brevispinus (1), Pisaster ochraceus (1), Psammechinus (1), Pycnopodia (1), Solaster (1), Strongylocentrotus (5), Tilapia (1), trout (1), Xenopus borealis (1), Xenopus laevis (5), chicken (7), cow (1), duck (2), human (11), mouse (4), and rat (2). Both mRNA and genomic DNA sequences were analyzed. Nucleotide sequences were aligned by using Clustal X (Thompson et al. 1997
) and checked visually for any possible errors afterwards. We have also used histone-like gene sequences from Euryarchaeota to study the origin of histone classes H1, H2A, H2B, H3, and H4 in eukaryotes. The representative sequences of eukaryotic histones from human, Drosophila, Arabidopsis, yeast, and Giardia were used for this purpose. A list of species names, sequence identifications, and GenBank accession numbers are available at http://mep.bio.psu.edu/databases.
The extent of nucleotide divergence was estimated by using the uncorrected p distance (Nei and Kumar 2000
). The proportions of synonymous (pS) and nonsynonymous (pN) differences per site were computed by the modified Nei-Gojobori method (Zhang, Rosenberg, and Nei 1998
). Phylogenetic trees were constructed by the neighbor-joining (NJ) method (Saitou and Nei 1987
). All analyses were conducted by using the computer program MEGA, Version 2.1 (Kumar et al. 2001
). The H4 gene of Giardia lamblia was used to root the tree for eukaryotic genes, as the Giardia lineage is believed to be the first to diverge from all other eukaryotes (Roger et al. 1998
; Wu et al. 2000
).
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Amino Acid Sequence Divergence
Histone proteins are classified into two different types based on their expression patterns: replication-dependent (RD) and replication-independent (RI) histones. RI histones are expressed continuously throughout the cell cycle, whereas RD histones are expressed only during the S-phase. However, H4 is the only histone protein that does not generally exhibit amino acid differences between RD and RI histones (Grimes et al. 1987
; Akhmanova, Miedema, and Hennig 1996
). The only species known to have distinct RI and RD protein sequences is the fungus Aspergillus nidulans, where RI proteins differ by two amino acids from RD proteins. Interestingly, the RD H4 gene of Aspergillus has an intron in the same position as the RD H4 gene of Neurospora. This suggests that these genes are more closely related to each other than either one is to the H4 RI gene from Aspergillus. Similarly, RI and RD H4 genes appear to have separate evolutionary histories in species that possess identical RD and RI H4 protein sequences.
In most cases, there are only very few amino acid differences between H4 protein sequences of different species, even if the species are highly divergent (fig. 1
). For example, the H4 proteins from humans and the annelid worm Platynereis dumerilii show identical amino acid sequences (fig. 1
), even though these two species diverged almost 800 MYA (Nei, Xu, and Glazko 2001
). However, H4 proteins from the protist species used in this study display an unusually high level of sequence divergence (fig. 1 ). In this case, the majority of the variable sites are concentrated in the amino- and carboxyl-terminal regions of the protein. This relatively high level of divergence is not surprising if we note that the chromatin of these protist species does not condense during cell division (Aslund et al. 1994
; Espinoza et al. 1996
). Thus, purifying selection appears to be somewhat relaxed in the histone proteins of these species.
Nucleotide Sequence Divergence
The phylogeny of H4 genes based on nucleotide sequences is shown in figure 2
. The extent of overall nucleotide sequence divergence is substantially higher than that of protein sequence divergence. However, because H4 proteins show little sequence variation, pN is very low for most sequence comparisons (tables 1 and 2
). Consequently, most of the nucleotide sequence variation is in the form of synonymous substitution. The phylogeny presented in figure 2
shows that the genes from the same species do not necessarily cluster together. However, different clusters of the phylogenetic tree are weakly supported by the bootstrap test. This again suggests that the genes from a species are no more closely related to each other than they are to genes from a different species. For example, in human and Arabidopsis, the majority of intraspecific pS values are as high as the pS values between animal, plant, and fungi species. In contrast, pN values are very small even between different eukaryotic kingdoms (table 1
).
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In general, the extent of synonymous differences was very high both within and between species. The mean pS (
S) commonly ranged from 0.2 to 0.6 between genes from the same species (table 2
). In fact, synonymous substitutions have apparently reached the saturation level in many species, as shown by high pS values (0.4–0.74) for individual pairwise comparisons (Nei, Rogozin, and Piontkivska 2000
). Interestingly, the range of pS values was nearly the same for both within- and between-species comparisons. For example, S ranged from 0.3 to 0.6 in all vertebrates, except in chicken and duck (table 2 ). In fact, S was sometimes higher within species than between species. For example, S between human and mouse genes is smaller than S for intrahuman comparisons (0.480 and 0.542, respectively). Two frog species, X. laevis and X. borealis, which diverged about 15–20 MYA (Knochel et al. 1986
), exhibit interspecific clustering of putatively orthologous genes (fig. 2
and table 2 ).
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There are, however, some genes that show a low degree of intraspecific divergence at synonymous sites. For example, chicken and duck genes demonstrated low levels of H4 nucleotide sequence divergence. However, the level of divergence of the 5'- and 3'-flanking regions is rather high for the majority of these genes, considering the overall coding sequence identity (table 3 ). This and the fact that two pairs of chicken genes show a very high level of sequence similarity, even though they are located on the opposite DNA strands and separated by other histone genes, suggest that a recent gene duplication or gene conversion occurred, followed by an inversion to produce this high level of sequence similarity. However, the high sequence similarity in chicken and duck can also be attributed to an extremely high GC content in these genes, because the GC content at the third codon position is 95%–97%. A similar situation was observed in chicken and duck histone H3 genes (Rooney, Piontkivska and Nei 2002
). Therefore, we cannot exclude the possibility of gene conversion in these genes, but at this point it is difficult to distinguish between the hypotheses of concerted evolution and birth-and-death evolution in these genes. To settle the problem, a complete genome analysis of chicken and duck genes as well as those from other avian species would be necessary.
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Origin and Evolution of Histones H1, H2A, H2B, H3, and H4 in Eukaryotes
Eukaryotic genomes appear to be a chimera of eubacterial and archaebacterial genomes (Rivera et al. 1998
), and histone genes seem to be descendants of ancient archaebacterial genes because no histone-like genes were found in eubacterial species (Pereira et al. 1997
; Bailey et al. 2000
). In eukaryotes, there are five classes of histones, i.e., H1, H2A, H2B, H3, and H4; because most of the eukaryotic genomes contain all of these histone genes, they must have evolved before the diversification of eukaryotic kingdoms. However, the origin and the divergence of these genes are largely unknown. We therefore conducted a phylogenetic analysis of these genes using archaebacterial genes as outgroups. The phylogenetic tree obtained by using Poisson correction (PC) distance for amino acid sequences is presented in figure 3
. This tree shows that the five classes of histone genes are all monophyletic. However, the bootstrap support for the interior branches separating these five groups is rather low. This occurred partly because the number of amino acids used was small, but it is also possible that all five types of histone genes evolved nearly simultaneously, though the linker histone H1 might have arisen a little later. The latter hypothesis is also supported by the fact that the genome of one of the most primitive eukaryotes, Giardia, seems to be lacking H1 sequence (McArthur et al. 2000
; Wu et al. 2000
), though this can also be attributed to a gene loss event. Figure 3
also shows that histones H4 and H3 are the most conserved among all histone protein classes, whereas histone H1 is least conserved. This can be attributed to the crucial role of H3 and H4 proteins because the (H3 + H4)2 tetramers initiate the nucleosome assembly and comprise the structural homologs of archaeal nucleosome (Sandman, Pereira, and Reeve 1998
).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Our results suggest that the amino acid sequence similarity among histone H4 genes is maintained primarily by strong purifying selection rather than by concerted evolution. At the nucleotide level, the numbers of synonymous differences between member genes from the same species are generally very large and often near the saturation level. This high level of synonymous differences suggests that H4 genes are subject to birth-and-death evolution at the DNA level and that many genes have persisted in the genome for a long time. This is quite interesting, considering the fact that H4 proteins from distantly related species (e.g., human, trout, and chicken) are identical (fig. 1 ). This long-term conservation of protein sequences can only be explained by strong purifying selection.
If H4 genes evolve according to the model of birth-and-death evolution under strong purifying selection, pseudogenes may be generated (Nei and Hughes 1991
; Nei, Gu, and Sitnikova 1997
). Indeed, H4 pseudogenes have been found in X. laevis (Turner et al. 1983
), mice (Liu, Liu, and Marzluff 1987
; DeBry 1998
), humans (Kardalinou et al. 1993
; Albig and Doenecke 1997
), and Arabidopsis (Tacchini and Walbot 1995
). Our analysis of C. elegans genome has suggested that there is at least one H4 pseudogene. Some (i.e., Arabidopsis pseudogene) of these pseudogenes appear to have emerged quite recently, whereas others (e.g., human and C. elegans pseudogenes) seem to be quite old, as shown by the level of sequence divergence from other genes (table 4 ).
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We have shown that members of the histone H4 gene family do not evolve in a concerted manner in long-term evolution. Similar findings have also been reported in the highly conserved histone H3 family (Rooney, Piontkivska, and Nei 2002
) and the ubiquitin gene family (Nei, Rogozin, and Piontkivska 2000
). Furthermore, the model of birth-and-death evolution applies to many immune system gene families, such as the MHC (Nei and Hughes 1992
; Gu and Nei 1999
), immunoglobulin (Ota and Nei 1994
), TCR (Su and Nei 2001
), and ribonuclease genes (Zhang, Dyer, and Rosenberg 2000
), as well as other multigene families (Duda and Palumbi 2000
; Robertson 2000
). It appears that birth-and-death evolution is the major mode of evolution of multigene families in eukaryotes.
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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This work was supported by grants from NIH (GM20293) and NASA (NCC2-1057) to M.N.
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Footnotes |
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Fumio Tajima, Reviewing Editor
Present address: Department of Biological Sciences, P.O. Box GY, Mississippi State University 
Abbreviations: RD, replication dependent; RI, replication independent.
Keywords: histone H4
concerted evolution
birth-and-death evolution
purifying selection
Address for correspondence and reprints: Helen Piontkivska, Institute of Molecular Evolutionary Genetics, Pennsylvania State University, 328 Mueller Lab, University Park, Pennsylvania 16802. oxp108{at}psu.edu
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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 S. M. Mount, V. Gotea, C.-F. Lin, K. Hernandez, and W. Makalowski Spliceosomal small nuclear RNA genes in 11 insect genomes RNA, January 1, 2007; 13(1): 5 - 14. [Abstract] [Full Text] [PDF]
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 A. S. Novozhilov, G. P. Karev, and E. V. Koonin Biological applications of the theory of birth-and-death processes Brief Bioinform, March 1, 2006; 7(1): 70 - 85. [Abstract] [Full Text] [PDF]
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 G. F.J. ARMBRUSTER, M. BOHME, D. BERNHARD, and M. SCHLEGEL THE H3/H4 HISTONE GENE CLUSTER OF LAND SNAILS (GASTROPODA: STYLOMMATOPHORA): TS/TV RATIO, GC3 DRIVE AND SIGNALS IN STYLOMMATOPHORAN PHYLOGENY J. Mollus. Stud., November 1, 2005; 71(4): 339 - 348. [Abstract] [Full Text] [PDF]
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 Y. Li, C. Ye, P. Shi, X.-J. Zou, R. Xiao, Y.-Y. Gong, and Y.-P. Zhang Independent origin of the growth hormone gene family in New World monkeys and Old World monkeys/hominoids J. Mol. Endocrinol., October 1, 2005; 35(2): 399 - 409. [Abstract] [Full Text] [PDF]
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 Y. Go, Y. Satta, O. Takenaka, and N. Takahata Lineage-Specific Loss of Function of Bitter Taste Receptor Genes in Humans and Nonhuman Primates Genetics, May 1, 2005; 170(1): 313 - 326. [Abstract] [Full Text] [PDF]
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P. Pineau, M. Henry, R. Suspene, A. Marchio, A. Dettai, R. Debruyne, T. Petit, A. Lecu, P. Moisson, A. Dejean, et al. A Universal Primer Set for PCR Amplification of Nuclear Histone H4 Genes from All Animal Species Mol. Biol. Evol., March 1, 2005; 22(3): 582 - 588. [Abstract] [Full Text] [PDF]
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 C. M. Seabury, R. L. Honeycutt, A. P. Rooney, N. D. Halbert, and J. N. Derr Prion protein gene (PRNP) variants and evidence for strong purifying selection in functionally important regions of bovine exon 3 PNAS, October 19, 2004; 101(42): 15142 - 15147. [Abstract] [Full Text] [PDF]
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J. M. Eirin-Lopez, A. M. Gonzalez-Tizon, A. Martinez, and J. Mendez Birth-and-Death Evolution with Strong Purifying Selection in the Histone H1 Multigene Family and the Origin of orphon H1 Genes Mol. Biol. Evol., October 1, 2004; 21(10): 1992 - 2003. [Abstract] [Full Text] [PDF]
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N. Nikolaidis and M. Nei Concerted and Nonconcerted Evolution of the Hsp70 Gene Superfamily in Two Sibling Species of Nematodes Mol. Biol. Evol., March 1, 2004; 21(3): 498 - 505. [Abstract] [Full Text] [PDF]
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L. A. Katz, J. G. Bornstein, E. Lasek-Nesselquist, and S. V. Muse Dramatic Diversity of Ciliate Histone H4 Genes Revealed by Comparisons of Patterns of Substitutions and Paralog Divergences Among Eukaryotes Mol. Biol. Evol., March 1, 2004; 21(3): 555 - 562. [Abstract] [Full Text] [PDF]
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K. K. Kojima and H. Fujiwara Cross-Genome Screening of Novel Sequence-Specific Non-LTR Retrotransposons: Various Multicopy RNA Genes and Microsatellites Are Selected as Targets Mol. Biol. Evol., February 1, 2004; 21(2): 207 - 217. [Abstract] [Full Text] [PDF]
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