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An Evolutionarily Conserved Odontode Gene Regulatory Network Underlies Head Armor

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An Evolutionarily Conserved Odontode Gene Regulatory Network Underlies Head Armor bioRxiv preprint doi: https://doi.org/10.1101/2021.06.21.449322; this version posted June 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. An evolutionarily conserved odontode gene regulatory network underlies head armor formation in suckermouth armored catfish Shunsuke Moria,1 and Tetsuya Nakamuraa,1 Authors’ affiliations a Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, 08854, USA 1 Address correspondence to: Shunsuke Mori ([email protected]) and Tetsuya Nakamura ([email protected]) Running title: Odontode development in armored catfish Keywords: odontode, dermal denticle, suckermouth armored catfish Summary statement: Cranial dermal denticles in suckermouth armored catfish develop via an evolutionarily conserved and unique odontode genetic regulatory network. bioRxiv preprint doi: https://doi.org/10.1101/2021.06.21.449322; this version posted June 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 ABSTRACT 2 Odontodes, i.e., teeth and tooth-like structures, consist of a pulp cavity and dentine covered 3 by a mineralized cap. These structures first appeared on the outer surface of vertebrate 4 ancestors and were repeatedly lost and gained across vertebrate clades; yet, the underlying 5 genetic mechanisms and trajectories of this recurrent evolution remain long-standing 6 mysteries. Here, we established suckermouth armored catfish (Ancistrus sp.; Loricariidae), 7 which have uniquely evolved dermal odontodes (dermal denticles) all over most of their body 8 surface, as an experimental model animal amenable to genetic manipulation for studying 9 odontode development. Our histological analysis showed that suckermouth armored catfish 10 develop dermal denticles through the previously defined odontode developmental stages. De 11 novo transcriptomic profiling identified the conserved odontode genetic regulatory network 12 (oGRN) as well as unique expression of paired like homeodomain 2 (pitx2), previously 13 characterized as an early regulator of oGRN in teeth, in developing dermal denticles. 14 Knockdown of pitx2 perturbed formation of the epithelial placode of dermal denticles and 15 altered expression oGRN genes. By comprehensively identifying the genetic program for 16 dermal odontode development in suckermouth armored catfish, this work illuminates how 17 dermal odontodes independently evolved and diverged in distinct teleost lineages. 18 19 20 21 22 23 24 25 26 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.21.449322; this version posted June 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 27 28 INTRODUCTION 29 30 Exoskeletal armor is a prime protective adaptation for thriving in a natural environment, and 31 dermal odontodes are the most common exoskeletal feature found across the vertebrate 32 phylogeny of extinct and extant fish. Dermal odontodes are constructed from various types of 33 dentine sometimes covered by enamel/enameloid and primarily function as protectants and 34 ornaments on the vertebrate body (Janvier, 1996). They form body armor in concert with 35 underlying dermal bony plates in odontode-bearing fish, excepting modern cartilaginous fish 36 (Miyake et al., 1999). 37 During vertebrate evolution, the first dermal odontodes shielding the body surface 38 appeared in in Silurian (~460 million years ago) in pteraspidomorphi, extinct jawless fish 39 group including anaspids or heterostracans (Keating and Donoghue, 2016). Thereafter, 40 throughout the evolution of jawless and jawed fish, the architecture of odontodes with 41 underlying dermal bony plates has been continuously modified and displays extraordinary 42 morphological divergence (Keating et al., 2015). Odontodes may have been recruited into the 43 oral cavity and transformed into teeth in the “outside-in” model during the origin of jawed 44 fish (Reif, 1982a). However, due to gaps in the fossil record, the evolutionary origin of teeth 45 continues to be disputed and revisited (Berio and Debiais-Thibaud, 2021; Fraser et al., 2010; 46 Witten et al., 2014). 47 Extant chondrichthyans (cartilaginous fish) and some species of primitive 48 actinopterygians (ray-finned fishes, e.g. gars and bichirs) and sarcopterygians (lobe-finned 49 fish, e.g., coelacanth) retain dermal odontodes on the body surface in the forms of placoid 50 scales or ganoid scales (Huysseune and Sire, 1998; Reif, 1982b; Williamson, 1849; 51 Williamson, 1851). However, dermal odontodes were lost in the early divergence of teleosts 52 (the largest infraclass in actinopterygians) and sarcopterygians; thus, most of them no longer bioRxiv preprint doi: https://doi.org/10.1101/2021.06.21.449322; this version posted June 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 53 have these structures. Intriguingly, dermal odontodes independently re-emerged as 54 convergent evolution in four living teleost groups: Xiphioidae (swordfish), Denticeps 55 (denticle herring), Atherion (pickleface hardyhead), and Loricarioidae (armored catfish) 56 (Fierstine, 1990; Sire and Allizard, 2001; Sire and Huysseune, 1996; Sire et al., 1998). In 57 these fishes, dermal odontodes on the extraoral skin display the conserved odonotode 58 organization and components, e.g., a pulp cavity surrounded by a dentin cone but without an 59 enamel cap. The exceptional resemblance of dermal odontode architectures among these 60 fishes implies a redeployment of the genetic network for odontode formation from existing 61 teeth or resurrection of the genetic program for lost dermal odontodes in each lineage, yet 62 little is known about the genetic basis underlying odontode convergent evolution in teleosts. 63 The developmental process of odontodes and its core set of regulatory genes were 64 uncovered principally by studying mammalian tooth formation. Tooth development begins 65 with epithelial placode formation; the thickened epithelium with reduced cell proliferation 66 functions as a signaling center, expressing the transcription factor paired like homeodomain 2 67 (pitx2) as well as genes encoding secreted factors, e.g., sonic hedgehog (shh), fibroblast 68 growth factors (fgfs), bone morphogenic proteins (bmps), and wnt (Bei et al., 2000; Bitgood 69 and McMahon, 1995; Chen et al., 2009; Dassule and McMahon, 1998). Via these diffusible 70 molecules, the placode triggers the sequential and reciprocal epithelial-mesenchymal 71 interactions and regulates formation of the tooth primordium, i.e., tooth germ, through the 72 well-defined developmental stages of bud, cap, bell, and eruption (Balic and Thesleff, 2015; 73 Thesleff and Tummers, 2008). 74 Recent comparative studies established histological and genetic links between teeth 75 and various dermal odontodes. For example, placoid scales, the dermal odontodes of 76 cartilaginous fish, form through the strictly conserved bud, cap, bell, and eruption stages 77 (Debiais-Thibaud et al., 2015). Also, shh, wnt, bmp, fgf and other genes indispensable for 78 tooth development are expressed in a comparable manner during both tooth and placoid scale bioRxiv preprint doi: https://doi.org/10.1101/2021.06.21.449322; this version posted June 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 79 formation (Cooper et al., 2017; Cooper et al., 2018; Debiais-Thibaud et al., 2015; Debiais- 80 Thibaud et al., 2011). These architectural and molecular correspondences between tooth and 81 dermal odontode development supports the classical hypothesis that genetic cascades were 82 co-opted from dermal odontodes to teeth (or vice versa). However, due to the lack of 83 experimental model animals amenable to genetic manipulation, there is little direct 84 experimental evidence for this hypothesis and, more broadly, for how odontodes are recruited 85 into novel tissues. 86 The catfish order (Siluriformes) offers a remarkable and unique opportunity to 87 understand the evolutionary mechanisms of dermal odontodes. The last common ancestor of 88 catfish is thought to have lost all body scales, but some lineages in the superfamily 89 Loricarioidea independently reverted to gain dermal odontodes, i.e., dermal denticles, 90 with/without underlying dermal bony plates (Haspel et al., 2012; Sire and Huysseune, 1996). 91 Although these dermal denticles in catfishes originated via convergent evolution, their 92 structures display the rigorously conserved odontode characteristics albeit lacking surface 93 enamel. The distribution of dermal denticles along the body in these catfish lineages is 94 evolutionarily diverse, occuring on the head, trunk, or both (Rivera-Rivera
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