Departamento de Biología Celular y Molecular, Universidade da Coruña, Campus de A Zapateira, A Coruña, Spain
Correspondence: E-mail: che{at}udc.es.
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Abstract |
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Key Words: birth-and-death evolution purifying selection concerted evolution histone H1 orphon genes
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Introduction |
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The H1 histone multigene family encodes linker proteins, which bind to the linker DNA in the chromatin fiber constituting the chromatosomal structure. There are multiple H1 isoforms, which have been best characterized in mammals whose complement consists of five somatic subtypes (H1.1 to H1.5), a tissue-specific subtype (H1t), a replacement subtype (H1°), and an oocyte-specific subtype (H1oo) (Albig et al. 1997; Wang et al. 1997; Tanaka et al. 2001). In nonmammalian species, there is a second differentiation-specific subtype (H5) related to H1° and expressed only in avian and amphibian nucleated erythrocytes (reviewed by Khochbin and Wolffe [1994]) and also another oocyte-specific H1 histone known as B4 or H1M (maternal) (Dimitrov et al. 1993). In invertebrates, the lower complexity determines the presence of fewer H1 isoforms, which are only defined by punctual changes of amino acid residues at specific positions. In the case of plants, many H1 genes possess intervening sequences (introns), the presence of polyadenylation signals in the mRNA is the rule rather than the exception, and there are several stress-inducible H1 subtypes (reviewed by Chabouté et al. [1993]).
Although the H1 multigene family is the fastest-evolving class among histones, H1 proteins are still highly conserved proteins and concerted evolution has been invoked to explain its evolution (Kedes 1979; Hentschel and Birnstiel 1981; Coen, Strachan, and Dover 1982; Ohta 1983; Hankeln and Schmidt 1993; Schienman, Lozovskaya, and Strausbaugh 1998). However, many multigene families do not fit the predictions made by the concerted-evolution hypothesis, and sequences of gene members are more closely related between than within species. To account for these observations, Nei and Hughes (1992) first proposed a new evolutionary model that they named the "birth-and-death" model of evolution. In this model, new genes are created by repeated gene duplication, and some of the duplicate genes are maintained in the genome for a long time, whereas others are deleted or become nonfunctional. Protein homogeneity is maintained by the effect of the strong purifying selection, and, consequently, DNA sequences of different members can be very different, both within and between species (Nei and Hughes 1992; Nei, Gu, and Sitnikova 1997; Nei, Rogozin, and Piontkivska 2000). This model has been reported as the primary mode of evolution for several multigene families, such as the major histocompatibility complex (MHC) (Nei and Hughes 1992; Gu and Nei 1999), immunoglobulin (Ota and Nei 1994), antibacterial ribonuclease genes (Zhang, Dyer, and Rosenberg 2000), nematode chemoreceptor gene families (Robertson 2000), ubiquitins (Nei, Rogozin, and Piontkivska 2000), T-cell receptor (Su and Nei 2001), histone 3 multigene family (Rooney, Piontkivska, and Nei 2002), histone 4 gene family (Piontkivska, Rooney, and Nei 2002), elapid snake venom three-finger toxins (Fry et al. 2003), plant MADS-box genes (Nam et al. 2004), and heat-shock 70 proteins from nematodes (Nikolaidis and Nei 2004). Although concerted evolution and birth-and-death evolution are conceptually different, they may not be distinguishable if the rate of concerted evolution is assumed to be very slow. In this work, we define concerted evolution as a rapid process of interlocus recombination or gene conversion so that even related species have different sets of homogeneous member genes (Dover 1982).
The purpose of this work is to provide a deeper insight into the long-term evolutionary pattern of the H1 multigene family through the evaluation of the relative importance of gene conversion, point mutation, and selection using the above criteria. In this sense, the presence of such independent RI H1 variants represents an invaluable tool used to test whether concerted evolution or birth-and-death evolution guides the long-term evolution of the H1 multigene family. The present contribution completes the molecular evolutionary characterization of the H1 histone multigene family and its orphon variants discussed in two previous reports by Eirín-López et al. (2002, 2004).
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Materials and Methods |
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Phylogenetic trees were reconstructed using the neighbor-joining (NJ) tree-building method (Saitou and Nei 1987). The reliability of the resulting topologies were tested by the bootstrap method (Felsestein 1985) and by the interior-branch test (Rzhetsky and Nei 1992; Sitnikova 1996), which produced the bootstrap probability (BP) and confidence probability (CP) values, respectively, for each interior branch in the tree. Because the bootstrap method is known to be conservative, BP > 80% was interpreted as high statistical support for interior branches in the tree, CP = 95% was otherwise considered statistically significant (Sitnikova, Rzhetsky, and Nei 1995). We rooted phylogenetic trees using the H1 gene of the protist Entamoeba histolytica, as it represents one of the most primitive eukaryotes for which an H1-related protein has been characterized (Kasinsky et al. 2001).
The GenBank database and complete genome databases (chicken, human, mouse, rat, Drosophila, nematode, sea urchin, Arabidopsis, corn, tomato, and wheat) were screened for the presence of H1 pseudogenes using the Blast tool (Altschul et al. 1990). The presence of truncated or incomplete H1 sequences, indels in the conserved protein central domain, as well as the absence or interruption of the major H1 5' promoter elements were viewed as pseudogenization features used to define putative H1 pseudogenes.
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Results |
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H1 Nucleotide Evolution
An additional phylogeny for H1 genes was reconstructed from 146 nucleotide-coding sequences belonging to 55 species, shown in figure 2. It is important to note that our attention focuses more on the phylogenetic tree reconstructed from amino acid sequences because the topology obtained using nucleotide sequences is not very reliable, given that many gene comparisons within and between species are close or have even reached the saturation level. Although H1 is the least-conserved histone class, most of the observed nucleotide divergence is presented as synonymous variation, both within and between species (fig. 2).
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If the H1 histone multigene family has evolved according to the birth-and-death model of evolution, pseudogenes may have been generated. By comparing the nucleotide differences between pseudogenes and functional genes with the intraspecific nucleotide variation, it is likely that putative pseudogenes identified for C. elegans and A. thaliana have emerged quite recently because of their low divergence values and relatively short branches in the phylogeny. However, the previously reported X. laevis pseudogenes (Turner et al. 1983) and the putative pseudogene identified for L. esculentum seem to be older, given their significant sequence divergence with functional H1 genes and longer branch lengths (fig. 2 and table 3).
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Discussion |
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If there is an evolution through a rapid process of interlocus recombination or gene conversion, both pS and pN would acquire similar values. Our results show that the extent of pS is always significantly greater than that of pN in comparisons both within and between species (table 1), suggesting an extensive silent divergence among H1 genes. Additionally, most of the estimated intraspecific pS values are as high as the pS values obtained between species, even those belonging to different eukaryotic kingdoms (table 2). These results, rather than an important effect of interlocus recombination, best fit the birth-and-death model, where the nucleotide divergence among members of the multigene family will be observed primarily at the synonymous level and pairs of genes that were duplicated recently are expected to be closely related or even identical (Nei, Rogozin, and Piontkivska 2000). The only exception to this observation was presented by chicken H1 genes, which show high sequence similarity. A possible explanation for this high level of similarity could involve (1) the high GC content in these genes (GC at third codon positions is 84% to 91% in chicken H1 genes), (2) a recent gene duplication within a short period of time (not enough time could have elapsed to allow for the accumulation of nucleotide substitutions), or (3) a gene conversion event, which could not be completely discarded in this case.
As mentioned above, under the birth-and-death model of evolution with strong purifying selection, some of the duplicated genes may become pseudogenes. Until now, the only example of H1 pseudogenes was described in Xenopus laevis (Turner et al. 1983). In our screening of the databases, we did not find any RD or RI truncated H1 sequences. Nevertheless, it was possible to define putative pseudogenes in Caenorhabditis elegans, Arabidopsis thaliana, and Lycopersicon esculentum, based on their unusual sequence features. The absence of significant differences from functional H1 genes and the moderate lengths of the branches in the phylogeny (table 3 and fig. 2) suggest a recent loss of function in the case of putative H1 pseudogenes from C. elegans and A. thaliana, as was shown by Ota and Nei (1994) for immunoglobulin VH genes. Pseudogenes from X. laevis and the putative pseudogene from L. esculentum, which show significant differences with functional genes, seem to be otherwise quite old (table 3). In the case of X. laevis, pseudogenes show the longest branch lengths in the phylogeny (fig. 2), which agrees with the birth-and-death model and suggests that neither intergenic gene conversion nor unequal crossing-over play major roles in homogenizing these genes (Ota and Nei 1994). Because H1 histones are less conserved compared with core histones, to clearly identify pseudogenes becomes a very problematic issue. Nevertheless, the presence of pseudogenes is not an absolute "must-be" condition of the birth-and-death model of evolution if the remaining assumptions are satisfied (Nei and Hughes 1992; Nei, Gu, and Sitnikova 1997; Nei, Rogozin, and Piontkivska 2000).
The presence of clustered H1 RD variants and solitary H1 RI variants allows us to determine whether, as predicted by the concerted evolution model, clustered genes show evidence of interlocus recombination more often than solitary genes (Ohta 1983). Our results show that protein homogeneity is also maintained by strong purifying selection in RI subtypes, which keep their identities and are more closely related between species (figs. 13 ). In this case, the presence of functional constraints would also account for the homologies observed among RI proteins from vertebrates. At the nucleotide level, there is also an extensive silent divergence both within and between species, which is always significantly greater than the nonsilent divergence (table 1). Again, the presence of a significant effect of interlocus recombination at the protein level in RI H1 histones seems unlikely, being probable that RI variants, as RD variants, evolve following the birth-and-death model of evolution with strong purifying selection.
Origin and Long-Term Evolution of RI orphon H1 Genes
The phylogenies reconstructed in the present work show that neither the orphon H1 variant from the midge Chironomus thummi (Hankeln and Schmidt 1993) nor the polyadenylated H1 gene from the annelid Chaetopterus variopedatus (del Gaudio et al. 1998) are included in the monophyletic group gathering the RI variants (figs. 13). An RI status was proposed for the cases cited above on the basis of their solitary genomic organization, analysis of promoter regions, and presence of putative polyadenylation signals, but except for the sea urchin H1
histone (Lieber et al. 1988), this latter feature has been inferred from nucleotide sequences rather than by expression analyses. The results of our Northern blotting experiments on mussel Mytilus galloprovincialis RNA show the presence of polyadenylated H1 transcripts, which together with previous evidence (Eirín-López et al. 2002, 2004), will definitively demonstrate the RI status for a fraction of H1 genes in mussels.
An orphon origin was hypothesized to explain the evolutionary origin of the RI H1 subtypes from vertebrates, where the exclusion of these genes from the main histone repetitive units and consequently from the interlocus recombination or concerted evolution events, would account for the presence of this differentiation-specific subtypes solitary in the genome (Schulze and Schulze 1995). If the effect of concerted evolution on the long-term evolution of both RD and RI H1 subtypes is not significant, as revealed in the present work, it is then necessary to revisit this orphon origin hypothesis to fit it into the birth-and-death model of evolution. A brief scheme of the model of birth-and-death evolution (Nei, Gu, and Sitnikova 1997) is adapted to the concrete case of H1 genes in figure 4A. Following this model, the different H1 isoforms may have been generated by recurrent gene duplication/deletion events. Functional H1 proteins would evolve under a strong purifying selection determined by their critical structural and functional roles, which would be already operating at the time of divergence of the RI H1 genes before the differentiation between vertebrates and invertebrates, about 815 MYA (Feng, Cho, and Doolittle 1997). At the nucleotide level, H1 genes may diverge extensively through synonymous substitution events, being DNA sequences of different gene family members very different both within and between species (Nei and Hughes 1992; Nei, Gu, and Sitnikova 1997). This events proposed theoretically in figure 4A are precisely shown by real data in figure 4B. This "tree of life" shows the organization of H1 and core histone genes in model organisms as well as in many other genomes, indicating the modifications in histone organization with special attention to whether H1 genes are in the major repetitive units or solitary in the genome and if they show RI features as polyadenylation signals. The next step after the duplication events would involve the transposition of RI H1 genes to a solitary location in the genome, where they would continue their evolution in a new physical location and where new genes and pseudogenes would be generated. The presence of transposition and inversion events is very common in histone evolution, as revealed by the different histone gene orientations in the DNA strands, and a similar pattern of duplication and transposition events has been postulated to explain the long-term evolution of the multigene families of the vertebrate immune system (Sitnikova and Nei 1998).
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In the present work, we have shown that although the members of the H1 histone multigene family encode a set of highly conserved proteins, they do not evolve in a concerted manner. The diversification of the H1 isoforms is enhanced primarily by mutation and selection, where genes are subject to birth-and-death evolution with strong purifying selection. This model is able to explain not only the diversification of RD H1 genes but also the origin and long-term persistence of orphon RI H1 subtypes in the genome. It is likely that H1 genes have experienced a faster birth rate and an apparently slower death rate compared with H3 and H4 families (Piontkivska, Nei, and Rooney 2002; Rooney, Piontkivska, and Nei 2002), given the greater diversification of the H1 isoforms and the few pseudogenes detected. Nevertheless, the long-term evolution of the H1 genes may have paralleled that of core histone genes to maintain a coordinate regulation (Peretti and Khochbin 1997). It seems that multigene families such as histones, which have evolved to produce a large quantity of the same gene product, also evolve at long-term following the birth-and-death model of evolution.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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References |
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