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Tbx4/5 Gene Duplication and the Origin of Vertebrate Paired Appendages

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Tbx4/5 Gene Duplication and the Origin of Vertebrate Paired Appendages Tbx4/5 gene duplication and the origin of vertebrate paired appendages Carolina Minguillona,1, Jeremy J. Gibson-Brownb,2, and Malcolm P. Logana,3 aMedical Research Council-National Institute for Medical Research, The Ridgeway, Mill Hill, London, NW7 1AA, United Kingdom; and bDepartment of Biology, Washington University, 1 Brookings Drive, St. Louis, MO 63130 Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved November 2, 2009 (received for review September 16, 2009) Paired fins/limbs are one of the most successful vertebrate inno- 12). Both genes encode transcription factors that directly regu- vations, since they are used for numerous fundamental activities, late the expression of Fibroblast growth factor-10 (Fgf10) and including locomotion, feeding, and breeding. Gene duplication establish an FGF signaling loop that drives limb outgrowth (7, 9). events generate new genes with the potential to acquire novel To investigate the relationship betwen duplication of a single, functions, and two rounds of genome duplication took place ancestral, Tbx4/5 locus to give rise to separate Tbx5 and Tbx4 loci, during vertebrate evolution. The cephalochordate amphioxus di- and the acquisition of vertebrate paired appendages, we com- verged from other chordates before these events and is widely pared the functions of the amphioxus Tbx4/5 gene, and its used to deduce the functions of ancestral genes, present in single genomic regulatory landscape, to those of the mouse Tbx4 and copy in amphioxus, compared to the functions of their duplicated Tbx5 gene loci. A priori, one can envisage two alternative vertebrate orthologues. The T-box genes Tbx5 and Tbx4 encode scenarios to explain the origin of paired appendages following two closely related transcription factors that are the earliest factors duplication of the single Tbx4/5 gene. First, before duplication of required to initiate forelimb and hind limb outgrowth, respec- the Tbx4/5 gene, mutations within the coding region endowed tively. Since the genetic components proposed to be responsible the descendant paralogous genes, Tbx5 and Tbx4, with the for acquiring a trait during evolution are likely to be involved in the potential to initiate limb outgrowth; specifically, the proteins formation of that same trait in living organisms, we investigated acquired the ability to activate Fgf10 in the LPM. Second, that whether the duplication of an ancestral, single Tbx4/5 gene to give after the divergence of cephalochordates, mutation(s) in the rise to distinct Tbx4 and Tbx5 genes has been instrumental in the regulatory regions of the ancestral Tbx4/5 locus, led ultimately to acquisition of limbs during vertebrate evolution. We analyzed the expression of the vertebrate Tbx4 and Tbx5 genes in the early whether the amphioxus Tbx4/5 gene is able to initiate limb LPM before limb bud stages, when this tissue is competent to outgrowth, and assayed the amphioxus locus for the presence of initiate limb outgrowth (13, 14). To investigate this further, we limb-forming regulatory regions. We show that AmphiTbx4/5 is undertook two complementary approaches: first, we tested the able to initiate limb outgrowth and, in contrast, that the genomic potential of the amphioxus Tbx4/5 protein to initiate limb locus lacks the regulatory modules required for expression that outgrowth in the forelimbless Tbx5 conditional knockout mouse would result in limb formation. We propose that changes at the (10) and second, we tested the ability of the AmphiTbx4/5 and level of Tbx5 and Tbx4 expression, rather than the generation of mouse Tbx5 and Tbx4 genomic regions to drive gene expression novel protein function, have been necessary for the acquisition of in the early LPM by transient transgenesis experiments in the paired appendages during vertebrate evolution. mouse. evolution ͉ limb ͉ Tbx5 Results We have used our limb-rescue assay (11) to test the ability of the ince Ohno’s visionary hypothesis concerning the origin of amphioxus Tbx4/5 protein to initiate limb outgrowth. We gen- Svertebrate innovations by genome duplication (1), numerous erated three independent transgenic lines (Prx1-Amphi4/5#1–3) reports have been published supporting this concept (reviewed in which the expression of the full-length AmphiTbx4/5 cDNA in ref. 2). The cephalochordate amphioxus, a limbless extant was driven under the control of the Prx1 promoter (Fig. 1 A and invertebrate relative of the vertebrates (3), has been extensively B) (15) in early, presumptive forelimb, LPM. In these transgenic used to study the ancestral functions of genes, present in single lines the amphioxus gene is ectopically expressed in forelimbs as copy in amphioxus, that have been duplicated in the vertebrate well as in hind limbs (Fig. 2 A–C). Analysis of e17.5-rescued lox/lox lineage. Amphioxus exhibits many basal chordate characteristics, embryos (Tbx5 ; Prx1-Cre; Prx1-Amphi4/5) revealed that including the presence of a dorsal nerve cord, a notochord, and AmphiTbx4/5 is able to initiate and maintain limb outgrowth Љ Љ segmented paraxial mesoderm, but lacks many vertebrate char- (Fig. 2 A –C ) as judged by comparison to the ‘‘no-forelimb’’ Ј acteristics such as migratory neural crest cells, a cranium, or an phenotype of the Tbx5 conditional knock-out (Fig. 3A ). Skeletal endoskeleton (4). We sought to investigate the origin of one of preparations of these embryos showed that all of the skeletal the most successful vertebrate innovations, paired appendages, elements along the entire proximo-distal axis of the limb (scap- which include the pectoral and pelvic fins of fish and their derived homologues, the forelimbs and hind limbs of tetrapods. Author contributions: C.M., J.J.G.-B., and M.P.L. designed research; C.M. and M.P.L. per- The T-box genes Tbx4 and Tbx5 are paralogous genes that formed research; C.M. and M.P.L. analyzed data; and C.M., J.J.G.-B. and M.P.L. wrote the arose by duplication of a single, ancestral Tbx4/5 gene. Extant paper. amphioxus possesses a single Tbx4/5 gene (AmphiTbx4/5) (5) and The authors declare no conflict of interest. lacks paired appendages, whereas all jawed vertebrates with two This article is a PNAS Direct Submission. pairs of paired appendages have distinct, postduplication Tbx4 Data deposition: The sequence reported in this paper has been deposited in the GenBank and Tbx5 genes. In vertebrates, Tbx5 is expressed in the lateral database (accession no. EU084005). plate mesoderm (LPM) of the presumptive pectoral fin/forelimb 1Present address: Consejo Superior de Investigaciones Cientificas, Instituto de Biologia region, whereas Tbx4 is expressed in the pelvic fin/hind limb Molecular de Barcelona. c/ Baldiri i Reixac, 10, 08028 Barcelona, Spain. region (reviewed in ref. 6). Tbx5 and Tbx4 are the earliest factors 2Present address: Institute for Evolutionary Discovery, 909 Hiawatha Drive, Mount Pleasant, required for the initiation of limb outgrowth (7–10), and are MI 48858. sufficient to initiate outgrowth in an otherwise limbless state (11, 3To whom correspondence should be addressed. E-mail: [email protected]. 21726–21730 ͉ PNAS ͉ December 22, 2009 ͉ vol. 106 ͉ no. 51 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0910153106 Downloaded by guest on September 30, 2021 Fig. 1. Cloning of the amphioxus Tbx4/5 cDNA. (A) Alignment of the deducted amino acid sequence of the AmphiTbx4/5 protein to the mouse Tbx5 and Tbx4 proteins. The N-terminal domain is underlined in blue, the T-domain is underlined in red, and the C-terminal domain is underlined in green. (B) Schematic representation of the Prx1-driven transgenic lines (15). (C) Schematic representation of the Tbx5 and Tbx4 genomic regions cloned in the BGZA reporter vector (16). e1, exon1; e2, exon2; i1, intron1; i2, intron2. ula, stylopod, zeugopod, and autopod) were present in the mouse regulatory regions required to drive expression of Tbx5 in AmphiTbx4/5-rescued limbs (Fig. 2 AЉ–CЉ). The extent of rescue, forelimb LPM and Tbx4 expression in hind limb LPM. To this from partial (Fig. 2B) to complete (Fig. 2 A and C) is presumably end, we cloned genomic DNA fragments that span regions dependant on the amount of AmphiTbx4/5 protein expressed in upstream of exon3 of the murine Tbx5 and Tbx4 genes into the each independent line. No effect of ectopic amphiTbx4/5 was LacZ reporter vector BGZA (Fig. 1C) (16) for transient trans- observed in the hind limb (Fig. 2 AЉ–CЉ). As additional controls, genesis assays in the mouse. Regulatory elements present Ͻ12 we generated transgenic lines in which the mouse Tbx4, Tbx5, or Kilobase pairs (Kb) upstream of exon3 of the mouse Tbx5 gene chimeric, domain-swap forms of Tbx4 and Tbx5, were driven by are sufficient to drive expression of the LacZ reporter in the e9.5 EVOLUTION the same Prx1 promoter. All of the rescued embryos for these forelimb LPM (Fig. 4A). Similarly, regulatory sequences Ͻ11 Kb genotypes had forelimbs (Fig. 3) consistent with Tbx4 and Tbx5 upstream of exon3 of mouse Tbx4 are sufficient to drive expres- having common roles in limb initiation, but not having roles in sion of the reporter in the e9.5 hind limb LPM (Fig. 4B). When limb-type specification (11). From these experiments, we con- an equivalent region from the AmphiTbx4/5 locus (Bf4/5–10) was clude that the single AmphiTbx4/5 gene product has the ability used for transgenesis, expression of the reporter in the mouse to initiate limb outgrowth when expressed at the correct time and LPM was never observed (0/12 positive transgenic embryos). To in the appropriate tissue (i.e., the prelimb bud stage LPM). determine whether any LPM-regulatory region was located These data demonstrate that mutations at the level of the coding further away from the amphioxus Tbx4/5 gene, we assayed a sequence cannot account for the limb-forming potential of the bacterial artificial chromosome (BAC; CH302 78M15) contain- mouse and other vertebrate Tbx5 and Tbx4 proteins.
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