Evolutionary relationships and diversification of barhl genes within retinal cell lineages
© Schuhmacher et al; licensee BioMed Central Ltd. 2011
Received: 12 June 2011
Accepted: 21 November 2011
Published: 21 November 2011
Basic helix-loop-helix and homeodomain transcription factors have been shown to specify all different neuronal cell subtypes composing the vertebrate retina. The appearance of gene paralogs of such retina-specific transcription factors in lower vertebrates, with differently evolved function and/or conserved non-coding elements, might provide an important source for the generation of neuronal diversity within the vertebrate retinal architecture. In line with this hypothesis, we investigated the evolution of the homeobox Barhl family of transcription factors, barhl1 and barhl2, in the teleost and tetrapod lineages. In tetrapod barhl2, but not barhl1, is expressed in the retina and is important for amacrine cell specification. Zebrafish has three barhl paralogs: barhl1.1, barhl1.2 and barhl2, but their precise spatio-temporal retinal expression, as well as their function is yet unknown.
Here we performed a meticulous expression pattern comparison of all known barhl fish paralogs and described a novel barhl paralog in medaka. Our detailed analysis of zebrafish barhl gene expression in wild type and mutant retinas revealed that only barhl1.2 and barhl2 are present in the retina. We also showed that these two paralogs are expressed in distinct neuronal lineages and are differently regulated by Atoh7, a key retinal-specific transcription factor. Finally, we found that the two retained medaka fish barhl paralogs, barhl1 and barhl2, are both expressed in the retina, in a pattern reminiscent of zebrafish barhl1.2 and barhl2 respectively. By performing phylogenetic and synteny analysis, we provide evidence that barhl retinal expression domain is an ancestral feature, probably lost in tetrapods due to functional redundancy.
Functional differences among retained paralogs of key retina-specific transcription factors between teleosts and tetrapods might provide important clues for understanding their potential impact on the generation of retinal neuronal diversity. Intriguingly, within teleosts, retention of zebrafish barhl1.2 and its medaka ortholog barhl1 appears to correlate with the acquisition of distinct signalling mechanisms by the two genes within distinct retinal cell lineages. Our findings provide a starting point for the study of barhl gene evolution in relation to the generation of cell diversity in the vertebrate retina.
The vertebrate retina is organized into a complex network of cell layers, namely the ganglion cell layer (GCL) which contains retinal ganglion cells (RGCs) and displaced amacrine cells (ACs), the inner nuclear layer (INL) which consists of ACs, horizontal, bipolar and Müller glia cells, and the outer nuclear layer (ONL) which is made up of cone and rod photoreceptors. This strikingly complex architectural plan of the retina is extremely well conserved across vertebrate species, probably in direct correlation with the conservation of the key regulatory factors that govern retinal development. Several members of the basic helix-loop-helix (bHLH) and homeodomain family of transcription factors are known to play a role in the determination of retinal progenitor competence and cell fate, a function that is highly conserved from fish to mammals . Much less is known on the contribution of different functional paralogs of retina-specific transcription factors, which arose subsequently to rounds of whole genome duplication (WGD) during vertebrate evolution . Indeed, it has been proposed that after WGD, duplicated genes can either accumulate loss-of-function mutations and are functionally lost (non-functionalization [3, 4]) or acquire a new function (neo-functionalization), or split the ancestral function between the paralogs (sub-functionalization) ), therefore adding complexity to the developmental gene network that shapes organ formation. The genes of the barhl family encoding the homeobox transcription factors Barhl1 and Barhl2, have been shown to be expressed in more or less overlapping domains of the central nervous system and have partially redundant functions in neural subtype cell identity, migration and survival [5, 6]; however, barhl2 members appear to be uniquely expressed in the retina [7, 8]. In particular, Barhl2 is a pan-vertebrate regulator of the specification and survival of ACs and RGCs [9–11]. Forced expression of Barhl2 in the mouse retina promotes the differentiation of glycinergic amacrine cells at the expense of bipolar and Müller cells . Additionally, analysis of Barhl2-null retinas suggests that Barhl2 plays a critical role in both AC subtype determination and in RGC survival . The Xenopus Barhl2 ortholog (previously named Xbh1) has been shown to be expressed in RGCs and in presumptive AC precursors, and to promote RGC differentiation downstream of the bHLH transcription factor Atoh7 . While Xenopus, mouse, rat and human have one copy of barhl1 and barhl2 each, zebrafish has three barhl paralogs possibly due to a further genome duplication event that teleosts underwent during evolution after the split from the tetrapod lineage [12, 13]. On the basis of protein sequence alignment and phylogenetic analysis, it has been suggested that two of these orthologs belong to the barhl1 paralog group (nominated barhl1.1 and barhl1.2) while the third belongs to the barhl2 group [6, 12]. In contrast to mouse and Xenopus, all three barhl seem to be expressed both in the brain and in the retina . In medaka fish (Oryzias latipes), only one barhl has been described so far (olbarhl); based on phylogenetic analysis olbarhl has been clustered to the barhl1 group of paralogs [6, 12, 14]. To get more insights into the evolution of barhl paralogs with respect to retinal differentiation we took advantage of the zebrafish and medaka model systems to perform a comprehensive comparative analysis of barhl gene expression as compared to the one in tetrapod. By detailed in situ hybridization analysis we confirmed that barhl1.2 and barhl2 are expressed in the zebrafish retina but not barhl1.1. A meticulous inspection of barhl1.2 and barhl2 transcript distribution indicates that while barhl2 appears to recapitulate the expression of its mammalian and Xenopus counterpart, the spatio-temporal expression pattern of barhl1.2 is non redundant to that of barhl2, suggesting that barhl1.2 might have evolved non redundantly with respect to barhl2 in the retina. Interestingly, we have detected that barhl1.2 shows a very early onset of expression which is highly overlapping with the expression of the atoh7 gene demarcating the onset of RGC genesis. Furthermore, we also describe a new barhl paralog in medaka which, based on protein alignment, could be assigned to the Barhl2 group. By comparing the expression of medaka barhl1 and barhl2, we found that they are both expressed in the retina, in a pattern reminiscent of zebrafish barhl1.2 and barhl2 respectively. These results combined with phylogenetic and synteny analysis suggest that barhl retinal expression domain is an ancestral feature that has been specifically lost in tetrapod probably due to functional redundancy following the duplication-supplementation paradigm [3, 4].
Zebrafish barhl1.2 and barhl2, but not barhl1.1, are expressed in distinct spatio-temporal domains of the developing retina
Expression of barhl1.2 and barhl2 in the retina suggests distinct regulation by atoh7
Identification of a novel barhl paralog in medaka
Conserved gene synteny between barhl genes
According to this study, we propose that vertebrates have two homologs of barhl (barhl1 and barhl2) due to WGD events that occurred before the emergence of vertebrates. This is in contrast with Drosophila, where two BarH genes probably arose from tandem duplication in the same locus. It is a topic of speculation whether there have been one or two rounds of WGD in early vertebrate evolution before the split of the teleosts from the other jawed vertebrates, and currently the most widely accepted view is that there were two [29, 30]. Our findings are consistent with the latter view as the third paralog found in zebrafish most likely originated from the additional round of whole genome duplication that marked the rise of teleosts and did not affect other vertebrates . This hypothesis is in agreement with the fact that in basal deuterostomes such as sea squirt and amphioxus, only one barhl locus could be found by BLAST search. From this speculation one would assume that all teleost fish once had at least three, maybe even four paralogs of barhl, some of which were lost. We found that in zebrafish both barhl2 and barhl1.2 are expressed in the developing retina. Barhl1.1, like other vertebrate barhl1 homologs, is not expressed in the retina whereas the medaka barhl1 and barhl2 are both expressed in the retina in a similar fashion as barhl1.2 and barhl2 in zebrafish, thus suggesting that medaka barhl1 has a similar dynamic of transcriptional regulation as zebrafish barhl1.2. Given that the barhl expression in the retina is an ancestral feature that was already present in Drosophila, the most parsimonious explanation for barhl1 gene evolution is that its retinal expression was maintained within the teleost lineage but was lost in Xenopus and mammals. Thereafter within teleosts, the zebrafish barhl1.1 also lost its retinal expression probably due to a redundant function with barhl1.2 and relaxed evolutionary pressure in its locus. This can be further illustrated in the context of the Tetraodon barhl1 paralogs. These sequences do only resemble partial or split Barhl proteins and therefore the positions in the tree are excluded from the teleost barhl1 cluster. We have called the split sequences Tetraodon Barhl1.2 and Barhl1.3 and the protein that clusters within the teleost group Barhl1.1. In contrast, Barhl2 protein sequences are arranged in correspondence with the evolution of the species, while the retinal expression of Barhl2 has been conserved throughout the animal kingdom. This could be related to changes in function or regulation of barhl1 paralogs that led to diversification and, in some cases, retention rather than loss of a duplicate. Unfortunately, without access to expression information for Tetraodon and stickleback, no further hypothesis on the relationship of function and copy number can be made.
In line with these observations, our in situ hybridization analysis suggests that the zebrafish barhl2 expression pattern closely resembles that of barhl2 ortholog in other vertebrates, and therefore might play a role in the same neuronal lineages. The mouse Barhl2 takes part in the specification of the ACs, and later aspects of RGC maturation [9, 10]. Functional experiments will be necessary to test this hypothesis in zebrafish. It also remains to be demonstrated whether the expression of barhl2 within the GCL is restricted to displaced ACs or RGCs or both, and whether part of barhl2 expression might be dependent on atoh7, like in other vertebrates . As the expression of atoh7 and barhl2 are mostly complementary, our hypothesis is that barhl2 transcriptional activation in the AC lineage is independent from Atoh7. Other candidate factors might be at work in inducing barhl2, particularly those factors that have been shown to favour AC fate at the expense of RGCs in zebrafish . The striking complementary expression of atoh7 and barhl2 that we observed (see Figure 4) would rather supports a negative feedback between the two genes. Interestingly, similar mutually excluding expression domains have been found also in Drosophila between the homolog atonal and bar genes . In this study, a negative feedback has been shown to occur between the two Drosophila genes, thus suggesting the conservation of an ancestral feature. The expression of barhl2 in the zebrafish atoh7-/- retina at 40 hpf appears to be retained in time but its pattern of expression is shifted towards the lens (Figure 5B). Most ACs born at this stage become displaced in the presumptive GCL (which is devoid of RGCs, ); which might account for the localization of barhl2 expression in this domain. Thus, our current data doesn't provide, neither it excludes evidences for negative feedback between atoh7 and barhl2 in zebrafish. In contrast to barhl1.1, we found that barhl1.2 is expressed in the zebrafish retina. Surprisingly, this expression occurs nearly in synchrony with the one of atoh7 and the development of RGCs. Similarly, we found that the medaka barhl1 spatio-temporal expression is reminiscent of what has been previously described for atoh7 expression in the medaka retina, being first detected at stage 25 and becoming restricted to the CMZ at stage 30-35 . This observation further supports the hypothesis of conserved dynamics of retinal lineages specification in both fish "twins", at least with respect to atoh7 and barhl genes. Thus, due to this extreme similarity between barhl1.2 and atoh7 expression within the RGC lineage, it is also possible that Barhl1.2 function became redundant with respect to the one of Atoh7 and was therefore lost in the tetrapod lineage. In light of this intriguing hypothesis, it will be very interesting to ask what is the retained function of the zebrafish barhl1.2 in the RGC lineage and in relation to atoh7.
After branching of the metazoan clades into protostomes and deuterostomes, a tandem replication in Drosophila melanogaster led to the existence of two Bar factors in the fruit fly that are assumed to be redundant. In other insects, such as Drosophila ananassae, Anopheles or Apis melifera, only one Bar can be found (results of TBLASTN search). In the line of the deuterostomes, at least one round of WGD took place before the rise of the gnathostomes (jawed vertebrates). We assume that before this period of intense genome rearrangement, there was only one Barhl, as we can find in the genome sequences of Branchiostoma floridae (amphioxus) or Ciona savignyi (sea squirt, results of TBLASTN search). Going further up in the evolutionary tree, at least two Barhls could be found in every species we looked at. These observations raise the intriguing hypothesis that Barhl factors have evolved in complexity proportional to the evolving diversity of retinal arrangement and rhabdomeric photoreceptor-derived cell types . In summary, our study provides an example on how retained gene paralogs might have evolved in contributing to the specification of distinct cell-lineages in the vertebrate retina. A larger scale analysis of the functional implications of the differences in retinal key transcription factors between teleosts and other vertebrates will help to speculate further on the role of duplication retention in the evolution of vertebrates, and more specifically during eye evolution.
In summary, our teleost comparison of Barhl orthologs highlights differences in expression patterns within retinal cell populations and regarding Atoh7 regulation. By extensive cross-species analysis of the barhl loci, these differences could be linked to differential selective pressure: while the barhl2 locus remains under evolutionary constraint, we show that the barhl1 locus rapidly evolves, thereby leading to functional differences within barhl1 paralogs. Our cross-species analysis provides insights on how retained gene paralogs might have evolved in relation to distinct cell-lineages in the vertebrate retina.
Breeding and rising of zebrafish followed standard protocols . Zebrafish embryos were treated with 0.0045% 1-Phenyl-2-Thiourea (PTU) in medium after gastrulation to prevent pigment formation. Medaka embryos were kept in ERM medium containing 1 g/l NaCl, 30 mg/l KCl, 40 mg/l CaCl2 × 2 H2O and 163 mg/l MgSO4 × 7 H2O in deionized water.
All fish are housed in the fish facility of our laboratory, which was built according to the local animal welfare standards (Tierschutzgesetz 111, Abs. 1, Nr. 1) and in accordance with European Union animal welfare guidelines. The facility is under the supervision of the local representative of the animal welfare agency. No animal experiments were performed. Embryos of medaka (Oryzias latipes) and zebrafish (Danio rerio) were used exclusively at stages prior to hatching (not considered as animals according to German law and European union regulations). Zebrafish and medaka were raised and maintained as described previously . The following strains were used for zebrafish embryos: wild type WIK/AB and for medaka embryos: the Cab wild type strain."
Amplification and cloning of medaka Barhl2
An 800 bp fragment was polymerase chain reaction (PCR)-amplified from mixed stage medaka cDNA eye and brain using the forward primer (GAGATAGACACCGTGGGAACTGG) and reverse primer (CTGATGGAGTCCGGTACATGCTG) designed to bind in exons 1 and 4 of olbarhl2 (ENSORLT00000002844, EnsEMBL v58). Cycling conditions: five cycles 95°C, 10 sec, 65°C, 20 sec, 72°C, 4 min; followed by 28 cycles with annealing at 60°C. A Taq DNA-Polymerase was used for A-Tailing, incubation was for 30 min at 72°C. The PCR product was cloned into pCRII TOPO TA vector (Invitrogen) and sequenced using T7 and SP6 promoters. The sequence has been submitted to the EMBL [GenBank: JQ008931].
Whole-mount in situ hybridization
Single whole-mount in situ hybridization of barhl genes was carried out as previously described in , for the zebrafish embryos and in , for the medaka embryos. Riboprobes where labelled with digoxigenin-UTP (Roche Applied Science). Hybridization with the probe was carried on over night at 65°C/68°C. Anti-DIG primary antibody coupled to alkaline phosphatase (Roche Molecular Biochemicals) and NBT-BCIP (Roche Molecular Biochemicals) was used for signal detection. For the FISH on zebrafish embryos, modifications were applied to the method described in , as suggested by Stephan Kirchmaier (unpublished). Embryos were washed with 100 μl Tyramide Signal Amplification (TSA) solution and incubated with FITC in TSA. Incubation with the barhl2 probe was for 30 minutes, incubation with the atoh7 probe was for 40 minutes. Embryos were then kept in the dark for all following steps. For detection and staining of the antisense probes, embryos were washed 5 × 10 min with TNT (0.1M Tris pH7.5, 0.15M NaCl, 0.1% Tween20), incubated with 1% H2O2 in TNT for 20 min and washed again 5 × 10 min. Embryos were blocked in TNB (2% DIG Block in TNT) for 1 h at RT and afterwards incubated with Anti-Digoxigenin-POD Fab fragments diluted 1:100 in TNB. For signal detection, Fluorescein (FITC), Cyanine 3 (Cy3) or Cyanine 5 (Cy5) Fluorophore Tyramide by PerkinElmer was used. Embryos were then incubated in 1 × 4',6-Diamidin-2-phenylindol (DAPI) in TNT over night at 4°C and washed several times in TNT the next day. Embryos stained with NBT/BCIP were mounted in 87% Glycerol on microscope slides and imaged with a Leica DM5000B, 10x or 20x air objectives, Leica CD500 microscope camera and Leica FireCam 1.7.1 software. Double fluorescent embryos were mounted in 100 × 15 mm glass bottom dishes in 1.5% low melting agarose. Confocal stacks were taken using the Leica SP5 confocal microscope, 20x water immersion objective and Leica Application Suite (LAS) software. FITC was excited at 488 nm by Argon laser, Cy3 by the 568 nm Helium-Neon laser, Cy5 at 633 nm by Helium-Neon and DAPI by an UV laser. Emission was sensed at 500-550 nm for FITC, 650-700 nm for Cy3, 650-800 nm for Cy5 and 400-500 nm for DAPI. Emission channels were imaged sequentially to avoid bleed-through of the two fluorescent signals. Pictures were processed using the open source software ImageJ version 1.43 and Adobe Photoshop CS3.
Protein sequences were obtained from EnsEMBL Genome Browser (v58) after using TBLASTN to perform a search for the zebrafish protein sequence of Barhl2 and Barhl1.1, respectively, against the genomic DNA of the used species to check the integrity of the annotated protein sequences. The following protein sequences were used: Danio rerio Barhl1.1 (Accession number ENSDARP00000016114) Danio rerio Barhl1.2 (Acc. No. ENSDARP00000051473) Danio rerio Barhl2 (Acc. No. ENSDARP00000093436) Homo sapiens BARHL1 (Acc. No. ENSP00000263610) Homo sapiens BARHL2 (Acc. No. ENSP00000359474) Mus musculus BARHL1 (Acc. No. ENSMUSP00000053147) Mus musculus BARHL2 (Acc. No. ENSMUSP00000084005) Xenopus tropicalis barhl1 (Acc. No. ENSXETP00000013720) Xenopus tropicalis barhl2 (Acc. No. ENSXETP00000051744) Gasterosteus aculeatus Barhl1 (ENSGACP00000023974) Gasterosteus aculeatus Barhl2 (ENSGACP00000005730) Tetraodon nigroviridis Barhl2 (ENSTNIP00000016761) Tetraodon nigroviridis Barhl1.1 (ENSTNIP00000008103) Tetraodon nigroviridis Barhl1.2 (ENSTNIP00000008179) Tetraodon nigroviridis Barhl1.3 (ENSTNIP00000008783) Takifugu rubripes Barhl1 (ENSTRUP00000013477) Takifugu rubripes Barhl2 (ENSTRUP00000032575) Oryzias latipes Barhl1 (Acc. No. ENSORLP00000015485) Ciona savignyi Barhl (ENSCSAVP00000019219) Drosophila melanogaster Bar1 (Acc. No. FBpp0074204) Drosophila melanogaster Bar2 (Acc. No. FBpp00742043) Sequences obtained from National Center for Biotechnology's (NCBI) GenBank database (Release 178): Xenopus laevis Barhl1 (Acc. No. AAG14451.1) Xenopus laevis Barhl2 (Acc. No. NP_001082021.1) Salmo salar Barhl1 (Acc. No. NP_001167081.1) Branchiostoma floridae Barhl1 (XP_002596391.1). The protein sequence of Oryzias latipes Barhl2 was obtained from translating the sequenced cDNA clone using the ExPASy online translate tool from Swiss Institute of Bioinformatics (SIB). Alignment of the sequences was produced using MUSCLE online at the European Bioinformatics Institute (EBI) . A phylogenetic tree was assembled using BioNJ online at phylogeny.fr performing 1000 bootstraps and using Jones-Taylor-Thornton matrix. This distance-based algorithm is claimed to be well suited for comparison of sequences with high substitution rates [36, 37]. The tree was visualized using the open source software Dendroscope .
Chromosomal loci of barhl genes in human, zebrafish, stickleback, Tetraodon and medaka were compared by identifying all genes that occur in more than one of the loci. The position of each of these genes was then searched in all species using the EnsEMBL database search function (EnsEMBL release v58). Position and identity of genes were plotted schematically according to their order and orientation (Figure 9, not to scale). Exact position of each gene can be found in the Additional file 1: Table 1.
We would like to thank S. Kirchmaier for providing the double FISH protocol; M. Eichenlaub for providing the medaka cDNA and helping with the in situ hybridization; B. Wittbrodt, E. Leist, A. Saraceno, M. Majewski, B. Seiferling, T. Kellner, L. Schertel, C. Mueller for fish maintenance and technical assistance. We are grateful to L. Ettwiller, M. Eichenlaub, P. Jusuf, G. Lupo, M. Carl, W.A. Harris, S. Schneider and J. Wittbrodt for discussion and suggestions on the manuscript, and to J. Wittbrodt for generous support. SA is funded by LGFG (Funding program of the State of Baden-Württemberg). This work was supported by the DFG (Eigenen Stelle to LP).
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