Veterinary Molecular Biology, Marsh Labs, Montana State University
Correspondence: E-mail: eschmidt{at}montana.edu.
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Abstract |
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Key Words: transcription TFIID cyclostome minisatellite duplication polypeptide genesis
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Introduction |
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The tetrapod TBP N-terminus can be divided into four subdomains (fig. 1a). Two of these, entitled NN and NC, which do not resemble each other or other known proteins, flank a central glutamine-rich repeat region, called Q. Near the junction with the conserved C-terminus is an imperfect repeat region of sequence (PXT)n, where X is generally M, A, or I. This repeat exists in most or all metazoan TBPs, and we suspect it serves as a connector that integrates phyla-specific properties of the various metazoan N termini with the universal functions of the C-terminus.
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The physiological site of the defect in these mice, the chorionic placenta, is found only in therian mammals. However, the presence of a similar TBP N-terminus among all tetrapods suggests this domain confers a fitness advantage on nonplacental as well as placental tetrapods. To gain insights into the preplacental functions of this domain, we isolated TBP cDNAs from strategically placed representatives of nontetrapod vertebrate lineages (teleost, shark, lamprey, and hagfish) and from an advanced nonvertebrate deuterostome (amphioxus). Within the resolution afforded by analyses of extant species, this domain was precisely restricted to vertebrates. Comparisons between species revealed that multiple events involving intragenic duplication of oligopeptide-encoding DNA sequences have occurred and persisted in this domain.
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Materials and Methods |
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For screening zebrafish and shark libraries, a cDNA probe containing most of the C- terminus and 222 bp of 3' untranslated region (UTR) of mouse (m) TBP was used. For screening lamprey and amphioxus libraries (8 x 105 to 10 x 105 phage screened per library), we used a mixed-species probe containing the same mTBP cDNA fragment and (1) an 840-bp Hinc II/Sca I fragment of shark TBP cDNA (144 bp of N-terminus, entire C-terminus, and 149 bp of 3' UTR); and (2) a 697-bp fragment of zebrafish TBP cDNA (start codon to a position midway through the C-terminus). TBP-containing inserts were recombined into SK- plasmid vectors and inserts were sequenced in both directions. Five amphioxus, two lamprey, two shark, and five zebrafish TBP cDNA clones (designated aTBP, lTBP, sTBP, and zfTBP, respectively) were sequenced.
We isolated 23 TBP clones from 1.8 x 106 plaques of the hagfish library (designated hfTBP); however none were full length. The two longest cDNAs encoded the entire C-terminus, but only 91 aa of the N-terminal region. The sequence revealed Pst I, Hind III, and Eco RI sites in the 5' end of the C-terminal protein-coding DNA. Genomic Southern blots suggested that the hagfish gene also contained Pst I, Eco RI, and Hind III sites at approximately 2.2 kb, approximately 3.5 kb, and approximately 6.7 kb upstream of the TBP N-terminal/C-terminal junction, respectively. Using Hind III ligation-mediated PCR (hfTBP-specific primer: 5'-TAT GGA TCC TGA CGT TGT GCT TCC ACT G-3'), we isolated and cloned a 1,359-bp genomic fragment, including more of the TBP N-terminal region. This fragment contained two exons, which, together, encoded a protein domain homologous to the entire exon 3encoded N-terminal region of mTBP. It did not, however, include the region homologous to mTBP exon 2, (start codon and subsequent 17 aa) (Sumita et al. 1993; Ohbayashi et al. 1996). A primer to sequences from the 5' protein-coding region of this clone (5'-TAT GGA TCC AGC ATC TAG TTG GTT CTG CC-3') was used in combination with the vector-encoded T3 primer to screen 24 portions (1 x 106 phage/portion) of the hagfish library by PCR. Two portions contained full-length hfTBP cDNAs, including 200 bp of 5' UTR.
Sequence Alignments, dN and dS Estimations, and Relatedness Predictions
Initial pair-wise alignments were performed using Blast (NCBI/GenBank). Progressive multiple sequence alignments were performed using ClaustalW software (Thompson, Higgins, and Gibson 1994) and best-fit/gap-placement was confirmed manually (fig. 1) (Thompson, Higgins, and Gibson 1994). dN/dS estimations were performed with the MEGA version 2.1 software package (Kumar et al. 2001) using five methods (Li, Wu, and Luo 1985; Nei and Gojobori 1986; Li 1993; Pamilo and Bianchi 1993; Comeron 1995) that differ in their treatment of transition versus transversion substitutions and their treatment of different-fold degenerate sites (Nei and Kumar 2000), as described in table 1. Relatedness was predicted on nucleotide sequences derived from gap-free polypeptide alignments as the Jukes-Cantor correction of p-distance for nonsynonymous substitutions using the modified Nei-Gojobori method (Nei and Kumar 2000) within MEGA 2.1. Relatedness is presented in figure 2 as distance trees built using the UPGMA Tree Making method (Kumar et al. 2001) within MEGA 2.1. Best-fit, gap-free N-terminal alignments between vertebrate and lower metazoan species were nearly arbitrary because no regions of homology are identifiable outside the PXT region (e.g., compare vertebrate and amphioxus sequences in figure 1b). Therefore, although the modified Nei-Gojobori method within MEGA 2.1 (Kumar et al. 2001) gave p-distance values, the tree in figure 2a is not drawn this deep because we did not wish to imply a common ancestry for these polypeptide domains.
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GenBank accession numbers are AY168624 to AY168633. Ten sequence files were deposited.
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Results |
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Although these results suggested that the TBP N-terminus was as conserved between tetrapods groups as was H2B, published data indicated that nonvertebrate species, including nematodes, insects, and echinoderms, lacked sequences resembling the tetrapod N-terminus (NCBI/GenBank) (Muhich et al. 1990; Tamura et al. 1991; Lichtsteiner and Tjian 1993). Therefore, we initiated a study aimed at determining which species between echinoderms and tetrapods contained sequences related to the tetrapod N-terminus.
Phylogenetic Distribution of the N-Terminus
TBP cDNAs were isolated from a cephalochordate (amphioxus), from two primitive jawless vertebrates (hagfish and lamprey), from a jawed cartilaginous fish (nurse shark), and from a teleost (zebrafish). Three TBP mRNA isoforms, encoding two protein isoforms, were isolated from amphioxus. The two proteins differed only by a GQ insertion/deletion within an XQ heterodipeptide repeat region (fig. 1b). In addition, three different 3' UTR isoforms were found, which differed by the presence or absence of oligonucleotide insertions (fig. 1c). Thus, as compared with the shortest isoform (number 1), isoform number 2 had four insertions of lengths 7, 8, 18, and 23 bp, respectively. Isoform number 3 lacked these insertions, but had two other insertions of lengths 4 and 7 bp. The 8-bp insertion in the former isoform, and the 7-bp insertion in the latter, are direct repeats of adjacent sequences; other oligonucleotide insertions resemble nearby sequences, suggesting that they might be diverged repeats.
The amphioxus N-terminus, like those of all metazoans, had a PXT repeat; however, outside of this region, it lacked sequences suggesting homology with either the tetrapod N terminus (fig. 1b) or with TBP domains in any more primitive metazoans (NCBI/GenBank [data not shown]). Conversely, zebrafish, shark, lamprey, and hagfish TBP N-termini resembled those of tetrapods (fig. 1b). Both within the C-terminal domain and within the NN region, hagfish and lamprey TBP proteins had shared amino acids that differed from those in higher vertebrates (fig. 1b). Phylogenetic relationship predictions based on either the N-terminus or the C-terminus grouped lamprey and hagfish within a clade and separated vertebrates from all lower metazoans (fig. 2). Nevertheless, the hagfish N-terminus was longer than those of other vertebrates, including lamprey, largely as a result of being interspersed with several additional oligopeptide domains (fig. 1b). A recent report of TBP cDNA sequences from a Pacific lamprey (Lethenteron reissneri) and medaka (Oryzias latipes) (Hoshiyama, Kuma, and Miyata 2001) is consistent with the lamprey and teleost sequences described here.
It was interesting that, although no single-nucleotide polymorphisms were found between the open reading frames of different hagfish clones, individual cDNAs encoded 11, 12, or 13 Q residues within the Q region. TBP Q repeat-length variation also occurs between individual humans, and this has been attributed to possible expansion/deletion of trinucleotide microsatellites (Rubinsztein et al. 1996; Koide et al. 1999; Yamada, Tsuji, and Takahashi 2000). Such repeat-length variation between individuals within a species, in the absence of any silent single-base polymorphisms, indicates that these Q-region expansions/contractions persist more frequently than do point mutations within the N-terminus. However, unlike some other Q-repeat regions, for example, in Huntingtin protein (Yamada, Tsuji, and Takahashi 2000), both Q-encoding codons (CAA and CAG) are found in the Q regions of tbp genes from most species, including hagfish (fig. 1b) (NBCI/GenBank). In the presence of frequent expansion/contraction of Q codons, the apparently low rate of point mutation is unlikely to account for Q codon heterogeneity. This suggests that the mechanism that alters the length of this domain does not tend toward fixation of one codon or the other (see Discussion).
The PXT repeat also varies in length between metazoan phyla, and since the repeat unit contains three different amino acids, repeat length variation cannot be easily explained by trinucleotide microsatellite duplications/deletions. Rather, it requires reiteration of larger ( 9 bp) minisatellites. Interestingly, hagfish exhibited one more PXT repeat than did other vertebrates, including lamprey (fig. 1b). Thus, the mechanism that alters the length of the TBP PXT repeat has been active at least once since divergence of hagfishes from lampreys.
Within the NN and NC regions of hagfish TBP, short motifs were found that were absent from other vertebrates (fig. 1b, amino acids 44 to 52 and 102 to 109). These domains each appear to be diverged tandem duplications of sequences immediately adjacent to them. Thus, the NC motif, TTALPSG, exists in two additional imperfect repeats in all species, and the NN motif is an apparent diverged duplication of the adjacent oligopeptide sequence (amino acids 53 to 61; consensus: ASTL
P
) (fig. 1b). At least one other region in the hagfish NN region, beginning at amino acid 36 (TGLTPQP), resembles the core of this repeat. This region is a part of the most highly conserved portion of the NN region, suggesting that this sequence is ancient and that its integrity is important.
Phylogenetic Distribution of Introns Within Sequences Encoding the N-Terminus
The positions of introns within genes are highly conserved during evolution (Long, de Souza, and Gilbert 1995; de Souza, Long, and Gilbert 1996; Gilbert, de Souza, and Long 1997). Although the TBP N-terminus in tetrapods is encoded almost entirely by a single large exon (Nakashima et al. 1995; Ohbayashi et al. 1996; Shimada et al. 1999), our analyses of tbp genomic sequences revealed an unexpected "extra" intron in this region of the hagfish tbp gene (see Materials and Methods). Analysis of genomic DNAs from the other vertebrates in our study indicated that lamprey also had an intron at this position; however, zebrafish and shark did not (fig. 3). This intron forms a phylogenetic marker that distinguishes hagfishes and lampreys, as a group, from all other vertebrates.
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Discussion |
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Vertebrate Phylogeny and the TBP N-Terminus
Although the phylogenetic position of hagfishes has been controversial (Janvier 1999; Neidert et al. 2001; Delarbre et al. 2002), a recent report based on mitochondrial genomes concluded that hagfishes and lampreys share a clade, "cyclostomata," within vertebrata (fig. 4) (Delarbre et al. 2002). Relatedness prediction algorithms for both the N-terminal and the C-terminal regions of TBP group the hagfish and lamprey polypeptides within a separate vertebrate clade (fig. 2). Moreover, hagfishes and lampreys, but not jawed vertebrates, have an intron at an identical position within the region encoding the N-terminus (fig. 3). Because the entire protein-coding regions of these genes are homologous to those of higher vertebrates, the designations for conserved (i.e., homologous) exons and introns should be retained. Therefore, we have designated this new intron "C" for "cyclostomata," the clade to which this intron is restricted. The exons on either side of intron C are designated "3-left" and "3-right" to indicate that they are homologous to the left and right sides of exon 3 from higher vertebrates, respectively. We cannot determine whether intron C arose immediately after divergence of the lineage leading to cyclostomes or was more primitive but was lost from the lineage leading to jawed vertebrates (fig. 4). Nevertheless, in combination, our TBP sequence data and the presence of the cyclostome-specific intron C support the proposed monophyletic origin of cyclostomes (Delarbre et al. 2002).
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Evolution of the Vertebrate TBP N-Terminus
The results presented here suggest the TBP N-terminus has undergone multiple events involving duplication of oligopeptide-encoding domains (fig. 1b). Expansion of heterodipeptide or larger repeats would likely require duplications of 6-bp, 9-bp, or larger minisatellite sequences. The 3' UTR sequences of individual TBP cDNAs from a polyclonal amphioxus population suggested that insertion/deletion of small minisatellite sequences occurs frequently in the tbp gene (fig. 1c). We also documented duplications in sequences encoding homooligopeptides (Q region), heterodipeptides (GQ polymorphism in amphioxus), heterotripeptides (PXT repeats), and larger heterooligopeptides (NN and NC repeats). A previous study noted the presence of several other 6-aa to 9-aa oligopeptide repeats within the TBP N-termini of C. elegans, Drosophila, and humans, and suggested that these repeats might function in transcription (Lichtsteiner and Tjian 1993). Here we propose a model by which duplication and divergence of oligopeptide units might have allowed de novo evolution of this vertebrate-specific polypeptide domain.
It is generally accepted that two major routes by which novel genes appear is by duplication and divergence of existing genes or by duplication, "shuffling," and divergence of existing exons (reviewed in Gilbert, de Souza, and Long 1997). Much less is known about the evolution of novel proteins or protein domains by other mechanisms. Our data suggest that, at or about the time of the appearance of the first vertebrates, the TBP N-terminus might have evolved de novo by duplications and divergence of minisatellite-encoded oligopeptide domains. Minisatellites are known to be major contributors to repetitive genomic regions (Heringa 1998). They have also been implicated in creating the repetitive polymorphisms within in the mucin genes (Fowler, Vinall, and Swallow 2001). We theorize that duplication and divergence of minisatellite repeats can also contribute to the genesis of novel polypeptide domains.
Regions of arbitrary length might be duplicated during replication, as has been proposed as a general mechanism for minisatellite expansion (Levinson and Gutman 1987). Indeed, only one of the six minisatellite insertions that we found in the amphioxus 3' UTRs (noncoding) was a multiple of 3 nt in length (fig. 1c). In protein-coding regions, modifications that altered the reading frame would disrupt the downstream TBP C-terminus and therefore would not persist. As a result, neither the nucleic acid sequence nor the amino acid sequence would need to have a deterministic effect on the reiterative mechanism, either in terms of reading-frame maintenance or in terms of the positions or lengths of the duplications. Rather, disruptive duplications or deletions would reduce fitness and would be lost from the lineage by natural selection. Modeling reveals that intragenic minisatellite duplications tend to tandemly reiterate amino acid motifs rather than introduce novel amino acids (fig. 5a). Once dimerized, subsequent duplications of the same size will add another repeat of the exact same unit even if they initiate out-of-step with the existing repeats (fig. 5b). The propensity of this mechanism to duplicate short oligopeptide-encoding domains suggests it could play an important role in creating many reiterative secondary structures, such as the B-ZIP domain (7-aa diverged-repeat helix) (Landschultz, Johnson, and McKnight 1988), the ankyrin repeat (33-aa diverged fold structure) (Bork 1993; Mosavi, Minor, and Peng 2002), the collagen repeat (GXP repeat), the C-terminal domain (CTD) repeat on the large subunit of RNA pol II (7-aa repeat) (Ahearn et al. 1987), and others.
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Functions of the TBP N-Terminus
Because all vertebrates, but no nonvertebrates, possess a TBP N-terminus that is globally homologous to that of tetrapods, this domain likely first appeared in an ancestor shared by all extant vertebrates but not by amphioxus (fig. 2). This suggests the vertebrate TBP N-terminus likely participates in functions that arose coincident with the earliest vertebrates and that it has imparted a fitness advantage on all subsequent vertebrate lineages.
Anatomically, the transition to vertebrates is correlated with the appearance of characteristics such as vertebrae, neural crest tissue, placodes, and others (Neidert et al. 2001; Delarbre et al. 2002). This transition was also associated with gene duplications leading to novel members of some developmental transcription factor families, including the Otx and Dlx families (Tomsa and Langeland 1999; Neidert et al. 2001), which participate in neural crest formation (Dolle, Price, and Duboule 1992; Vignali et al. 2000). However, the pathways in which these factors function (Simeone, Puelles, and Acampora 2002), as well as all of the known regulators and pathways that define neural crest (Baker and Bronner-Fraser 1997; Langeland et al. 1998; Neidert et al. 2001; Garcia-Castro, Marcelle, and Bronner-Fraser 2002; Knecht and Bronner-Fraser 2002), are far more ancient than is neural crest, per se. In the absence of a truly "vertebrate-specific" pathway regulating neural crest formation, it has been theorized that vertebrate-specific regulation of preexisting pathways allowed formation of this tissue uniquely in the vertebrate lineage (Baker and Bronner-Fraser 1997). In this light, it is interesting to consider that our work suggests the promoters of all genes in all vertebrates, but not in nonvertebrate phyla, are bound by TBP molecules that contain a unique N-terminal domain. In other words, all vertebrate transcription initiation complexes are "vertebrate-specific," not because of the DNA sequence of their promoters, but rather, because of this novel polypeptide domain within the basal transcription machinery.
The physiological functions for which natural selection has conserved this domain may differ between vertebrate phyla. Thus, although disruption of the TBP N-terminus in mice leads to a defect in therian pregnancy (Hobbs et al. 2002), no other vertebrates share this process, and, by inference, natural selection must have conserved this domain for other functions in pretherian vertebrates. These observations are consistent with model for evolution of this protein domain that we proposed based on functional studies in the mutant mice in which existing motifs can acquire novel activities that might later become "backed-up" to make the system robust (Schmidt et al. 2003). Since mice lacking the N-terminus exhibit only a defect in an evolutionary recent function, one might hypothesize that, if the N-terminus retains any of its more ancestral functions in mice, these can be accomplished by redundant mechanisms.
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Acknowledgements |
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Footnotes |
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