Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University
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Abstract |
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Introduction |
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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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Materials and Methods |
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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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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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Discussion |
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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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Acknowledgements |
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Footnotes |
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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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