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Deep Evolutionary Origin of Limb and Fin Regeneration

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Deep Evolutionary Origin of Limb and Fin Regeneration Deep evolutionary origin of limb and fin regeneration Sylvain Darneta,1, Aline C. Dragalzewa,1, Danielson B. Amarala,1, Josane F. Sousaa, Andrew W. Thompsonb, Amanda N. Cassc, Jamily Lorenaa,d, Eder S. Piresd, Carinne M. Costaa, Marcos P. Sousae, Nadia B. Fröbischf, Guilherme Oliveirad, Patricia N. Schneidera, Marcus C. Davisc, Ingo Braaschb, and Igor Schneidera,2 aInstituto de Ciências Biológicas, Universidade Federal do Pará, 66075-900 Belém, Brazil; bDepartment of Integrative Biology, Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI 48824; cDepartment of Biology, James Madison University, Harrisonburg, VA 22807; dInstituto Tecnológico Vale, 66055-090 Belém, Brazil; eLaboratório de Biologia Molecular, Museu Paraense Emílio Goeldi, 66077-530 Belém, Pará, Brazil; and fMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany Edited by Günter P. Wagner, Yale University, New Haven, CT, and approved June 11, 2019 (received for review January 10, 2019) Salamanders and lungfishes are the only sarcopterygians (lobe- data support the hypothesis that tetrapods inherited a limb re- finned vertebrates) capable of paired appendage regeneration, generation program from sarcopterygian fish ancestors (10). regardless of the amputation level. Among actinopterygians (ray- Among actinopterygians, teleosts, such as zebrafish, have been finned fishes), regeneration after amputation at the fin endoskel- broadly used for fin regeneration studies, yet their regenerative eton has only been demonstrated in polypterid fishes (Cladistia). abilities are thought to be limited to the dermal fin ray skeleton Whether this ability evolved independently in sarcopterygians and (11, 12). However, evidence of tail regeneration after endo- actinopterygians or has a common origin remains unknown. Here skeleton amputation has been shown in zebrafish (13). Thus far, we combine fin regeneration assays and comparative RNA-sequencing only 2 actinopterygian species, both from the earliest branching Polypterus (RNA-seq) analysis of and axolotl blastemas to provide ray-finned fishes, the Polypteridae, have been found to fully re- support for a common origin of paired appendage regeneration in generate paired fins, including the endoskeleton: the Senegal Osteichthyes (bony vertebrates). We show that, in addition to poly- bichir Polypterus senegalus (14, 15) and the ropefish Erpetoichthys pterids, regeneration after fin endoskeleton amputation occurs in calabaricus (15). Currently, our understanding of the evolution of extant representatives of 2 other nonteleost actinopterygians: the appendage regeneration is hindered by limited knowledge of the American paddlefish (Chondrostei) and the spotted gar (Holostei). Furthermore, we assessed regeneration in 4 teleost species and regeneration capabilities across fish clades. To address this, we show that, with the exception of the blue gourami (Anabantidae), assessed fin regeneration capacity in key taxa representing all ex- 3 species were capable of regenerating fins after endoskeleton am- tant major actinopterygian clades and examined gene-expression putation: the white convict and the oscar (Cichlidae), and the gold- profiles of limb and fin regenerating blastemas via RNA se- fish (Cyprinidae). Our comparative RNA-seq analysis of regenerating quencing (RNA-seq) in Polypterus. blastemas of axolotl and Polypterus reveals the activation of com- Here we provide evidence of regeneration after amputation at mon genetic pathways and expression profiles, consistent with a the fin endoskeleton in the American paddlefish (Chondrostei), shared genetic program of appendage regeneration. Comparison of RNA-seq data from early Polypterus blastema to single-cell RNA- Significance seqdatafromaxolotllimbbudandlimbregenerationstagesshows Polypterus that and axolotl share a regeneration-specific genetic Salamanders and lungfishes are the only lobe-finned verte- program. Collectively, our findings support a deep evolutionary brates where appendage regeneration after endoskeleton origin of paired appendage regeneration in Osteichthyes and provide amputation has been demonstrated. Here we show that an evolutionary framework for studies on the genetic basis of paired-fin regeneration after endoskeleton amputation occurs appendage regeneration. in living representatives of all major actinopterygian clades: the American paddlefish (Chondrostei), the spotted gar (Holostei), limb | fin | regeneration | tetrapod | evolution and in 2 cichlid and 1 cyprinid species (Teleostei). Through comparative transcriptome analysis of blastemas, we demon- typical osteichthyan paired fin (i.e., pectoral and pelvic fin) strate that axolotl and Polypterus deploy a similar genetic pro- Ais composed of an array of proximal fin radials (the endo- gram during regeneration. Furthermore, we show that early skeleton), followed distally by the fin rays (the dermal skeleton). blastemas in both species activate a common regeneration- The tetrapod limb evolved from paired fins in Devonian sar- specific genetic program. Collectively, our findings support a copterygians. During this transition, the fin ray dermal skeleton deep evolutionary origin of limb and fin regeneration and was lost and the elaborate limb endoskeleton emerged, consist- highlight the strengths of a comparative approach to identify ing of a proximal segment, the stylopod (humerus and femur), an genetic signatures of vertebrate appendage regeneration. intermediate segment, the zeugopod (radius/ulna, tibia/fibula), and a distal segment, the autopod (manus and pes) (1). There- Author contributions: S.D., A.C.D., D.B.A., J.F.S., A.W.T., A.N.C., N.B.F., M.C.D., I.B., and I.S. designed research; S.D., A.C.D., D.B.A., J.F.S., A.W.T., A.N.C., E.S.P., C.M.C., G.O., P.N.S., fore, whereas fin rays have no direct homologous counterpart in M.C.D., I.B., and I.S. performed research; S.D., J.L., E.S.P., C.M.C., M.P.S., G.O., P.N.S., tetrapod limbs, the limb endoskeleton and the endoskeletal el- M.C.D., and I.B. contributed new reagents/analytic tools; S.D., A.C.D., D.B.A., J.F.S., ements of fish paired fins share deep homology (2, 3) (Fig. 1A). A.W.T., A.N.C., J.L., E.S.P., M.P.S., N.B.F., G.O., P.N.S., M.C.D., I.B., and I.S. analyzed data; Among sarcopterygians, the capacity to regenerate the limbs and S.D., A.C.D., D.B.A., J.F.S., A.W.T., A.N.C., N.B.F., M.C.D., I.B., and I.S. wrote the paper. and fins after amputations severing the endoskeleton has been The authors declare no conflict of interest. reported only in 3 groups: frogs (4), salamanders (5), and lungfishes This article is a PNAS Direct Submission. (6). Although adult frogs cannot regenerate limbs, this capacity is Published under the PNAS license. exhibited by tadpoles before metamorphosis (7). Recent fossil ev- Data deposition: The sequences reported in this paper have been deposited in the NCBI idence has shown that limb regeneration occurred in basal am- Sequence Read Archive (project nos. PRJNA480693 and PRJNA480698). phibians before the emergence of stem salamanders, caecilians, and 1S.D., A.C.D., and D.B.A. contributed equally to this work. frogs; hence, this capacity is likely an ancient, plesiomorphic feature 2To whom correspondence may be addressed. Email: [email protected]. of tetrapods (8, 9). Recently, transcriptome analysis revealed strong This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. similarities between the transcriptional profiles deployed in lungfish 1073/pnas.1900475116/-/DCSupplemental. fin and salamander limb blastemas (LBs) (6). Altogether, current Published online July 3, 2019. 15106–15115 | PNAS | July 23, 2019 | vol. 116 | no. 30 www.pnas.org/cgi/doi/10.1073/pnas.1900475116 Downloaded by guest on September 29, 2021 A Fin/limb regeneration after endoskeleton amputation Present Dermal skeleton Absent Unknown Endoskeleton Endoskeleton (Mya) y 0 Gar Birds Frogs* Lizards Teleosts Lungfish Mammals Paddlefish Polypterids Coelacanth Salamanders Teleostei Holostei Cartilaginous fish Amniota Chondrostei Cladistia 300 Tetrapoda Dev Sarcopterygii Actinopterygii 400 Ord Sil Car Per day Present 500 EVOLUTION American paddlefish (P. spathula) Spotted gar (L. oculatus) B E Pectoral fin Pelvic fin Pectoral fin Pelvic fin C 28 dpa D 28 dpa F Before amputation G After amputation H 257 dpa I I’ Reg Uninjured J J’ Fig. 1. Phylogenetic distribution of appendage regeneration after endoskeleton amputation among vertebrates and of fin regeneration in nonteleost actinopterygians. (A, Upper) Schematic representation of endoskeleton and dermal skeleton of vertebrate appendages. (A, Lower) A time-calibrated ver- tebrate phylogeny depicts the state of current knowledge at the time this study was undertaken. Lineages containing one or more species capable of fin or limb regeneration after endoskeleton amputation are denoted in blue, those incapable denoted in orange, and those where no information exists in black. (B) Cleared and stained juvenile paddlefish at 75 dpf; pectoral and pelvic fins denoted. (C) Ventral view of a specimen with regenerated right pelvic fin at 28 dpa; arrowheads denote amputation site. (D) Ventral view of the cleared and stained specimen shown in C, displaying endoskeletal regeneration distal to the amputation site. (E) Spotted gar with pectoral and pelvic fins denoted. (F) Left pelvic fin before amputation. (G) Skeletal staining of fin removed by amputation; dotted line shows amputation site across the
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