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Genome Res. 14:11-17, 2004
©2004 by Cold Spring Harbor Laboratory Press; ISSN 1088-9051/04 $5.00
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Letter

Bichir HoxA Cluster Sequence Reveals Surprising Trends in Ray-Finned Fish Genomic Evolution

Chi-hua Chiu1,2,13, Ken Dewar3, Günter P. Wagner4, Kazuhiko Takahashi4, Frank Ruddle5, Christina Ledje6, Peter Bartsch7, Jean-Luc Scemama8, Edmund Stellwag8, Claudia Fried9,10, Sonja J. Prohaska9,10, Peter F. Stadler9,10,11 and Chris T. Amemiya12

1 Department of Genetics, Rutgers University, Piscataway, New Jersey 08854, USA 2 Center for Human Evolutionary Studies, Department of Anthropology, Rutgers University, New Brunswick, New Jersey 08901, USA 3 Department of Human Genetics, McGill University, Montreal, Quebec H3A1A4, Canada 4 Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520, USA 5 Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA 6 Department of Genetics, University of Lund, SE-223, Sweden 7 Museum für Naturkunde der Humboldt-Universität zu Berlin, D-10099 Berlin, Germany 8 Department of Biology, Howell Science Complex, East Carolina University, Greenville, North Carolina 27858, USA 9 Bioinformatics, Department of Computer Science, University of Leipzig, D-04103 Leipzig, Germany 10 Institute for Theoretical Chemistry and Structural Biology, University of Vienna, A-1090 Wien, Austria 11 The Santa Fe Institute, Santa Fe, New Mexico 87501, USA 12 Benaroya Research Institute at Virginia Mason, Seattle, Washington 98101, USA


   ABSTRACT
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The study of Hox clusters and genes provides insights into the evolution of genomic regulation of development. Derived ray-finned fishes (Actinopterygii, Teleostei) such as zebrafish and pufferfish possess duplicated Hox clusters that have undergone considerable sequence evolution. Whether these changes are associated with the duplication(s) that produced extra Hox clusters is unresolved because comparison with basal lineages is unavailable. We sequenced and analyzed the HoxA cluster of the bichir (Polypterus senegalus), a phylogenetically basal actinopterygian. Independent lines of evidence indicate that bichir has one HoxA cluster that is mosaic in its patterns of noncoding sequence conservation and gene retention relative to the HoxA clusters of human and shark, and the HoxA{alpha} and HoxA{beta} clusters of zebrafish, pufferfish, and striped bass. HoxA cluster noncoding sequences conserved between bichir and euteleosts indicate that novel cis-sequences were acquired in the stem actinopterygians and maintained after cluster duplication. Hence, in the earliest actinopterygians, evolution of the single HoxA cluster was already more dynamic than in human and shark. This tendency peaked among teleosts after HoxA cluster duplication.

Hox genes, which share sequence homology with the Hom-C genes of Drosophila and are clustered in the genome, form a distinct class of transcription factors that play an essential role in embryonic patterning (McGinnis and Krumlauf 1992Go). Hox clusters display the phenomenon of colinearity, in which the position of a gene in the cluster is related to its spatiotemporal pattern of expression along the anterior-posterior (A-P) axis (Lufkin 1996Go). Hox genes have a dynamic evolutionary history hallmarked by tandem (Kappen et al. 1989Go) and whole-cluster duplications (Holland and Garcia-Fernandez 1996Go; Ruddle et al. 1999Go). Whereas protostome taxa possess at most a single Hox cluster, the number of Hox clusters in different vertebrate lineages is varied (Ruddle et al. 1999Go). Vertebrate Hox clusters and their genes, therefore, are good models for identifying putative correlations between genomic and phenotypic evolution (Hughes and Kaufman 2002Go).

The ray-finned fishes (Actinopterygii; Fig. 1) are well suited to such studies. Teleost fishes (Nelson 1994Go) are the most diverse extant vertebrates, with >25,000 species. Moreover, the genomes of derived teleost fishes such as zebrafish, "euteleosts" sensu (Nelson 1994Go), contain duplicated genes of several different gene families (Postlethwait et al. 1998Go; Robinson-Rechavi et al. 2001Go; Taylor et al. 2001Go) and extra Hox clusters (Amores et al. 1998Go), as compared with their single orthologs in the genome of humans. The zebrafish (Danio rerio) possesses at least seven unlinked Hox clusters (A{alpha}, A{beta}, B{alpha}, B{beta}, C{alpha}, C{beta}, and D; Amores et al. 1998Go). Evidence for the presence of more than four Hox clusters also has been reported for additional euteleosts, including pufferfish (Takifugu rubripes; Aparicio et al. 2002Go; Amores et al. 2003Go), medaka (Oryzias latipes; Naruse et al. 2000Go), striped bass (Morone saxatilis; Snell et al. 1999Go), killifish (Fundulus heteroclitus; Misof and Wagner 1996Go), and tilapia (Oreochromis niloticus; Malaga-Trillo and Meyer 2001Go; Santini et al. 2003Go).



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  		Figure 1 Overview of jawed-vertebrate phylogenetic relationships with focus on the ray-finned fishes (Actinopterygii; Patterson 1982Go; Nelson 1994Go; Bartsch and Britz 1997Go; Bemis et al. 1997Go). The other two living sister groups to the ray-finnedfishes among gnathostomes are the cartilaginous (Chondrichthyes) andlobe-finned(Sarcopterygii) fishes, respectively. Note that only some euteleost clades are well represented to date, but remaining higher actinopterygian groups, Chondrostei (sturgeon and paddlefish), Neopterygii (gar, bowfin, and teleosts), andbasal teleost clades are virtually unresolved. This general outline of actinopterygian phylogeny is supportedin three of the most recent hypotheses basedon molecular data (Le et al. 1993Go; Venkatesh et al. 2001Go; Inoue et al. 2003Go). But, as with some conflicting morphologically basedhypotheses in the past, these also still indicate changing positions or lack of resolution among other basal actinopterygian fauna: sturgeon and paddlefish, gar, and bowfin.

 
In our recent analysis of patterns of noncoding sequence evolution in the duplicated HoxA{alpha} and HoxA{beta} clusters of zebrafish and in the single HoxA clusters of horn shark (Heterodontus francisci) and mammals, we proposed that following Hox cluster duplication, the noncoding control elements of zebrafish undergo extensive remodeling (Chiu et al. 2002Go). But, as indicated in Figure 1, there are several basal and intermediate actinopterygian lineages for which we do not, at present, have definitive knowledge on Hox cluster number. Hence, major questions remain. When, during ray-finned fish phylogeny, did the duplications that produced extra Hox clusters occur? Is the loss of Hox cluster noncoding sequence conservation observed in euteleosts also present in primitive actinopterygians? That is, is this phenomenon a characteristic of all ray-finned fishes, independent of duplication? How have Hox clusters evolved after duplication? To address these questions, we sequenced and analyzed the complete HoxA cluster of the bichir (Polypterus senegalus), a representative of the most basal extant ray-finned fish lineage as inferred from independent molecular data sets (Le et al. 1993Go; Venkatesh et al. 2001Go; Inoue et al. 2003Go) as well as its possession of ancestral morphological characters (Patterson 1982Go; Nelson 1994Go; Bartsch and Britz 1997Go; Bemis et al. 1997Go).


   RESULTS AND DISCUSSION
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 ABSTRACT
 RESULTS AND DISCUSSION
METHODS
 REFERENCES
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Bichir HoxA Cluster Architecture
We screened a BAC genomic library from P. senegalus and isolated a 180-kb HoxA contig spanning Evx1 to HoxA1 (Fig. 2). An additional HoxA cluster was not identified in our screenings. The architecture and gene complement of the HoxA cluster closely resemble that of the single HoxA clusters of human and horn shark (Kim et al. 2000Go; Chiu et al. 2002Go) and of the hypothetical gnathostome ancestor (Stellwag 1999Go). Disparate patterns of retention were observed for two medial group genes, HoxA6 and HoxA7. The bichir HoxA cluster encodes an intact HoxA6 gene, which has not been found in any euteleost examined. Remnants of the HoxA7 gene were observed in the bichir (Fig. 2A), similar to the situation observed in pufferfish (Amores et al. 2003Go). No obvious traces of an HoxA7 ortholog have been found in either the zebrafish HoxA{alpha} and HoxA{beta} clusters (Amores et al. 1998Go) or the pufferfish HoxA{beta} cluster (Fig. 2A; Aparicio et al. 2002Go; Amores et al. 2003Go). The HoxA{alpha} clusters of striped bass (Snell et al. 1999Go) and tilapia (Santini et al. 2003Go), on the other hand, each house an intact HoxA7 gene. Thus the HoxA7 gene has been independently lost in at least three distinct actinopterygian lineages, at least once in a basal group (bichir) and at least twice in teleosts (zebrafish, pufferfish). These two genes, HoxA6 and HoxA7, underscore that parallel events of gene losses within actinopterygians cannot be inferred solely on the basis of character reconstructions using parsimony.




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  		Figure 2 HoxA clusters and PFCs in human, shark, bichir, andeuteleosts. (Hs) Homo sapiens; (Hf) Heterodontus francisci; (Ps) Polypterus senegalus; (MsAa) Morone saxatilis HoxA{alpha}; (DrAa) Danio rerio HoxA{alpha}; (DrAb) D. rerio HoxA{beta}; (TrAa) Takifugu rubripes HoxA{alpha}; (TrAb) T. rubripes HoxA{beta}. (A) Hox genes are indicatedby blue rectangles. PFCs sharedexclusively between human andbichir are indicatedby green bars. PFCs sharedexclusively between bichir andeuteleosts are indicatedby coloredellipses. PFCs sharedbetween the HoxA{alpha} clusters of striped bass, zebrafish, and/or pufferfish are indicated by coloredtriangles. The PFC sharedbetween only zebrafish andpufferfish HoxA{alpha} clusters is indicated by a red diamond. The PFC shared between zebrafish andpufferfish HoxA{beta} clusters is indicated by an aqua blue circle. See text for description. (B) The co-occurrences of the PFCs in different clusters (Supplemental Table 1) can be representedas a tree. The height of an internal node is the average number of PFCs shared by two clusters in the two different subtrees. The position of the tips gives the total number of PFCs in the segment of the HoxA cluster that spans from Evx1 to HoxA1. The nonduplicated HoxA regions of human, shark, andbichir form one group. The secondsignificant group consists of the HoxA{alpha} sequences of the euteleosts. The position of the incomplete stripedbass (Morone saxatilis) sequence is estimatedby assuming that in a complete sequence we wouldhave foundroughly the same number of PFCs as in pufferfish (T. rubripes). The HoxA{beta} clusters are much further divergedanddo not appear to group together because euteleost-specific PFCs in the HoxA{beta} cluster are very rare (Supplemental Table 1). The smaller rate of PFC loss in the zebrafish HoxA{beta} cluster is the dominating effect.

 
Phylogenetic Analysis Supports a Single HoxA Cluster in the Bichir
Phylogenetic analyses of HoxA cluster coding sequences of human, shark, bichir, and euteleosts are consistent with the inference that the bichir has a single HoxA cluster (Figs. 3A-E). We examined trees for HoxA13, HoxA11, HoxA10, and HoxA2 amino acid sequences of shark (Kim et al. 2000Go), human (Venter et al. 2001Go), coelacanth (Koh et al. 2003Go; C. T. Amemiya and T. Powers, unpubl.), bichir (this study), zebrafish (Amores et al. 1998Go), and pufferfish (Fig. 3; Aparicio et al. 2002Go). The topology of a neighbor-joining tree of concatenated HoxA11 and HoxA13 exon 1 coding sequences indicates that the bichir and teleosts last shared a common ancestor prior to the duplication event that gave rise to the duplicated HoxA clusters in zebrafish and pufferfish (Fig. 3A). This leaves open the possibility that bichir has independently acquired an HoxA cluster duplication. To address this possibility, we examined the rate of nonsynonymous substitutions (Figs. 3B-E) because our earlier findings for the duplicated HoxA11{alpha} and HoxA11{beta} paralogs of zebrafish (Chiu et al. 2000aGo) showed that gene duplication is associated with an increased rate of replacement substitutions. Amino acid character reconstructions of HoxA13 (Fig. 3B), HoxA11 (Fig. 3C), and HoxA2 (Fig. 3E) confirm a higher rate of nonsynonymous substitutions for the duplicated paralogs of zebrafish and pufferfish. The orthologous bichir sequences accumulated significantly fewer amino acid changes (Figs. 3A-E). This finding is consistent with our library screening results and gene tree reconstructions indicating only a single HoxA cluster in bichir.







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  		Figure 3 Phylogenetic analysis andcharacter reconstructions of Hox coding sequences. (A) Neighbor-joining tree of concatenated HoxA13 and HoxA11 exon 1 coding sequences. Bootstrap support (1000 replications) for the euteleost nodes are shown. (Hf) Heterodontus francisci; (Lc) Latimeria chalumnae; (Ps) Polypterus senegalus; (TrAb) Takifugu rubripes HoxA{beta}; (DrAb) Danio rerio HoxA{beta}; (TrAa) T. rubripes HoxA{alpha}; (DrAa) D. rerio HoxA{alpha}. (B-E) Character reconstructions of exon 1 coding sequences under constraint trees for HoxA13, HoxA11, HoxA10, and HoxA2, respectively. Taxa abbreviations are as in A above, including (Hs) Homo sapiens. The indicated substitutions are only those that map unambiguously to the branches of the trees. The numbers of analyzedamino acidresidues andassumedunambiguous changes for each gene are (B) HoxA13, 244 amino acids and 196 steps; (C) HoxA11, 192 amino acids and 151 steps; (D) HoxA10, 24 amino acids and 35 steps; (E) HoxA2, 105 amino acids and 59 steps.

 
Noncoding DNA Sequence Comparisons Suggest the Single HoxA Cluster in Bichir Is Mosaic Between Human and Derived Ray-Finned Fishes
We next examined the evolution of noncoding sequences to determine whether the single HoxA cluster of bichir exhibits the dramatic loss of noncoding sequence conservation observed in the duplicated HoxA clusters of euteleosts (Chiu et al. 2002Go). We used a new software package, Tracker (Prohaska et al. 2003Go), to identify conserved Hox noncoding sequence tracts (potential cis-regulatory elements) in all the taxa shown in Figure 2A. Here, we report phylogenetic footprint clusters (PFCs; Chiu et al. 2002Go) of each HoxA cluster spanning from Evx1 to HoxA1 (Fig. 2A) counted by Tracker in pairwise sequence alignments of intergenic sequences between orthologous HoxA gene pairs (Supplemental Table 1). Figure 2B diagrammatically illustrates the number of PFCs that each pair of sequences (e.g., human, bichir) has in common. Several notable patterns of conservation of PFCs are evident. First, the HoxA clusters of human and horn shark share the most PFCs, consistent with our earlier findings (Chiu et al. 2002Go). Second, the bichir HoxA cluster shares 44 PFCs with horn shark and 40 PFCs with human; these numbers are much higher than the number of PFCs shared between any of the euteleosts and human and/or shark. A subset of these PFCs conserved between bichir and human are completely absent in euteleosts (Fig. 2A). Two extensive PFCs, of 11 total, shared exclusively between bichir and euteleosts (c49, c190 of Supplemental Table 1 available online at www.genome.org) are illustrated in Figure 2A. These observations indicate that the bichir exhibits a mosaic pattern of conservation of HoxA noncoding sequence tracts with human and derived actinopterygians. Third, the common ancestor of bichir and teleosts possessed cis-sequence elements that were largely acquired before the duplication and were retained in the duplicated HoxA{beta} clusters only. Most of the changes are located between Evx1 and HoxA13 (Fig. 2A; c36,37,38,47,49,50,54 of Supplemental Table 1), indicating that this modification was a single event. Fourth, 24 PFCs are shared only among the different euteleosts examined (Fig. 2A; Supplemental Table 1). Based on parsimony, these PFCs were uniquely derived in the stem lineage of euteleosts prior to the HoxA cluster duplication. We conclude that the loss of conservation in zebrafish, bass, and pufferfish is a derived state for teleost fishes and that the bichir is already more derived in its noncoding sequence than human and shark.

Conclusions
In this study we found independent lines of evidence indicating that the bichir has one HoxA cluster that is mosaic in its patterns of noncoding sequence conservation and gene retention relative to the single HoxA cluster of human and shark, and the duplicated HoxA{alpha} and HoxA{beta} clusters of zebrafish, pufferfish, and striped bass. Our findings show that the duplication that produced additional HoxA clusters in derived actinopterygians occurred after the bichir diverged from the rest of the ray-finned fishes (Fig. 1). Hence, it is important to investigate the genome situation in additional basal ray-finned fishes such as the paddlefish, bowfin, sturgeon, and gar, as well as basal teleosts such as the eel (Fig. 1). Some of the changes that distinguish zebrafish and fugu from human, however, were acquired prior to the teleost HoxA cluster duplication, as shown in the pattern of cis-sequence conservation between teleosts and bichir. Hence the divergence of actinopterygian Hox clusters from the gnathostome archetype already began before the duplication that produced duplicate Hox clusters in teleost fishes.

In this genome-enabled era, two major problems remain: how evolutionary forces such as mutation, duplication, and selection shape genomes, and how genomic variation relates to phenotypic alterations in different lineages. This study reinforces the view that the ray-finned fishes provide good opportunities for addressing these challenges. Comparisons on a genome-wide basis are urgently needed to understand the complex interactions between evolution of genomes and body plans in this speciose assemblage.


   METHODS
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 ABSTRACT
 RESULTS AND DISCUSSION
 METHODS
REFERENCES
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Construction and Screening of the Bichir BAC Genomic Library
A 5x coverage BAC genomic library, with an average insert size of 130 kb, was constructed for the bichir (P. senegalus) as described (Strong et al. 1997Go; Osoegawa et al. 1998Go). High-density 5 x 5 arrayed filters were made by the RZPD (http://www.rzpd.deGo). Hybridization using nonradioactive DIG-labeled probes was done following methods described in Chiu et al. (2000bGo). The first screen of this library was carried out using a pool of bichir (gift of C. Ledje and F. Ruddle; Ledje and Ruddle 2002Go) and coelacanth (gift of T. Powers [Benaroya Research Institute at Virginia Mason, Seattle, WA] and C. Amemiya) homeobox sequences isolated in genome-wide PCR surveys. This screen identified nine BAC clones of P. senegalus. A PCR survey of each BAC clone was done using a degenerate homeobox primer pair (334, 5'-GARYTIGARAARGARTTY-3'; 335, 5'-ICKICKRTTYT GRAACAA-3'). One clone containing the posterior part of the HoxA (Evx1, HoxA13, HoxA11, HoxA10) cluster was identified. Bichir HoxB, HoxC, and HoxD cluster sequences are presently being analyzed (C.-H. Chiu, K. Dewar, and P.F. Stadler, unpubl.).

To find overlapping BAC clone(s) that contain the rest of the HoxA cluster, PCR primers specific to bichir HoxA10 exon 1 were designed (PseA10F, 5'-ATGTCATGCTCAGATAGCCCGG-3'; PseA10R, 5'-TGATGTTTTGTATAAGGACATCG-3'). Using these primers, exon 1 of HoxA10 was amplified from whole-genomic DNA of the bichir (P. senegalus), cloned, and five independent colonies were sequenced on both strands. All five clones from genomic DNA were identical in sequence to each other and to the HoxA10 sequence on the BAC clones isolated using hybridization (described above). The PseA10F/R PCR primer pair was then used to PCR-screen DNA pools of the bichir BAC library (the library consists of 216 pools, with each pool equivalent to one 384-well plate). The screen with HoxA10 primers yielded two clones, the original BAC clone described above (containing Evx1 to HoxA10) and one overlapping clone, spanning HoxA10 to HoxA1. These two clones overlap ~4.0 kb encompassing the entire HoxA10 locus with 5'- and 3'-flanking sequences. Concurrent with PCR screening of the library pools, the 5 x 5 high-density filters of the bichir BAC library were also screened by hybridization, using bichir-specific HoxA10 exon 1 (from genomic DNA) as probe. Hybridization yielded the identical two HoxA cluster clones identified above that overlap over HoxA10. Finally, bichir HoxA2 exon 1 was amplified from genomic DNA (P. senegalus) using universal primers we designed (PseA2UF, 5'-AATAG TCAGCCR TCGCTYGCTGAG-3'; PseA2UR, 5'-CTTGGAHGCYTT TTTCTCKTTC-3'). The bichir HoxA2 exon 1 PCR product was cloned, sequenced, and used to screen the bichir BAC library filters by hybridization. Only one strong hybridization signal was detected, corresponding to the same BAC clone (spanning HoxA10 to HoxA1) identified above.

Phylogenetic Analyses
Phylogenetic reconstructions were conducted using the neighbor-joining method (Saitou and Nei 1987Go). Character reconstructions were done using MacClade Version 4.03 (Maddison and Maddison 2001Go) under constraint trees that retain bony fishes (ray-finned fishes and lobe-finned fishes) as monophyletic to the exclusion of horn shark. The indicated substitutions are only those that map unambiguously to the branches of the trees. Supplemental Table 2 contains the alignments used for phylogenetic tree reconstructions.

Noncoding Sequence Analyses
The program Tracker is based on BLAST (Altschul et al. 1990Go) searches of all possible sequence pairs. The resulting list of pairwise sequence alignments is then assembled into groups of partially overlapping regions that are subsequently passed through several filtering steps. There are three levels of resolution of conserved noncoding sequences that are analyzed. (1) Individual phylogenetic footprints (PFs) are blocks of 6 bp or more of DNA sequence 100% conserved in taxa that have an additive evolutionary time of 250 million years (Tagle et al. 1988Go). PFs are considered to be putative transcription-factor-binding sites. (2) Cliques (CCs) are groups of contiguous footprints (Prohaska et al. 2003Go). (3) Phylogenetic footprint clusters (PFCs; Chiu et al. 2002Go) are composed of at least two PFs that are separated by <100 nt. CCs and PFCs are considered to be putative enhancer/promoter regions.


   Acknowledgements
 
We are grateful to April Cook and the Whitehead Institute Center for Genome Research sequencing teams for the complete sequencing of the bichir HoxA cluster; and Tom Powers and Allan Force for discussion of portions of this manuscript. C.-H.C. and G.P.W. thank Austin Hughes for providing the SCR3 software. Funding for this research is gratefully acknowledged from the Busch Biomedical Research Fund to C.-H.C.; NSF IBN-9905403 to F.R. and G.P.W.; IBN-9905403 and NIH R24-RR14085 to C.T.A.; and DFG Bioinformatics Initiative BIZ 6/1-2 and FWF P#15893 to P.F.S.

The publication costs of this article were defrayed in part by payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 USC section 1734 solely to indicate this fact.


   Footnotes
 
Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.1712904.

13 Corresponding author.
E-MAIL chiu{at}biology.rutgers.edu; FAX (732) 445-1147. Back

[Supplemental material is available online at www.genome.org.]


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WEB SITE REFERENCES
 

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Received July 1, 2003; accepted in revised format October 30, 2003.
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