{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T11:24:19Z","timestamp":1782905059484,"version":"3.54.5"},"reference-count":64,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["R15GM139113-01A1"],"award-info":[{"award-number":["R15GM139113-01A1"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["P20GM103430"],"award-info":[{"award-number":["P20GM103430"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["R35GM147253-01"],"award-info":[{"award-number":["R35GM147253-01"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005562","name":"North Carolina Biotechnology Center","doi-asserted-by":"publisher","award":["2022-FLG-3803"],"award-info":[{"award-number":["2022-FLG-3803"]}],"id":[{"id":"10.13039\/100005562","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EvoDevo"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Cnidarians have become valuable models for understanding many aspects of developmental biology including the evolution of body plan diversity, novel cell type specification, and regeneration. Most of our understanding of gene function during early development in cnidarians comes from a small number of experimental systems including\n                    <jats:italic>Hydra<\/jats:italic>\n                    and the sea anemone,\n                    <jats:italic>Nematostella vectensis.<\/jats:italic>\n                    Few molecular tools have been developed for use in hard corals, limiting our understanding of this diverse and ecologically important clade. Here, we report the development of a suite of tools for manipulating and analyzing gene expression during early development in the northern star coral,\n                    <jats:italic>Astrangia poculata.<\/jats:italic>\n                    We present methods for gene knockdown using short hairpin RNAs, gene overexpression using exogenous mRNAs, and endogenous gene tagging using CRISPR-mediated gene knock-in. Combined with the fact that spawning can be induced in the laboratory, during the reproductive window, these tools make\n                    <jats:italic>A. poculata<\/jats:italic>\n                    a tractable experimental system for investigative studies of coral development. Further application of these tools will enable functional analyses of embryonic patterning and morphogenesis across Anthozoa and open new frontiers in coral biology research.\n                  <\/jats:p>","DOI":"10.1186\/s13227-025-00243-9","type":"journal-article","created":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T08:38:47Z","timestamp":1747384727000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Microinjection, gene knockdown, and CRISPR-mediated gene knock-in in the hard coral, Astrangia poculata"],"prefix":"10.1186","volume":"16","author":[{"given":"Jacob F.","family":"Warner","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan","family":"Besemer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alicia","family":"Schickle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erin","family":"Borbee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabella V.","family":"Changsut","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Koty","family":"Sharp","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leslie S.","family":"Babonis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,5,16]]},"reference":[{"key":"243_CR1","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/jmor.1050890103","volume":"89","author":"K Atoda","year":"1951","unstructured":"Atoda K. The larva and postlarval development of the reef-building corals IV. Galaxea aspera quelch. J Morphol. 1951;89:17\u201335.","journal-title":"J Morphol"},{"key":"243_CR2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2113701119","volume":"119","author":"LS Babonis","year":"2022","unstructured":"Babonis LS, Enjolras C, Ryan JF, Martindale MQ. A novel regulatory gene promotes novel cell fate by suppressing ancestral fate in the sea anemone Nematostella vectensis. Proc Natl Acad Sci. 2022;119: e2113701119.","journal-title":"Proc Natl Acad Sci"},{"key":"243_CR3","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1038\/s41467-023-36615-9","volume":"14","author":"LS Babonis","year":"2023","unstructured":"Babonis LS, Enjolras C, Reft AJ, Foster BM, Hugosson F, Ryan JF, Daly M, Martindale MQ. Single-cell atavism reveals an ancient mechanism of cell type diversification in a sea anemone. Nat Commun. 2023;14:885.","journal-title":"Nat Commun"},{"key":"243_CR4","doi-asserted-by":"publisher","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","volume":"30","author":"AM Bolger","year":"2014","unstructured":"Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114\u201320.","journal-title":"Bioinformatics"},{"key":"243_CR5","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1016\/S0278-4343(03)00080-3","volume":"23","author":"S Brooke","year":"2003","unstructured":"Brooke S, Young C. Reproductive ecology of a deep-water scleractinian coral, Oculina varicosa, from the southeast Florida shelf. Cont Shelf Res. 2003;23:847\u201358.","journal-title":"Cont Shelf Res"},{"key":"243_CR6","doi-asserted-by":"publisher","first-page":"19867","DOI":"10.1038\/srep19867","volume":"6","author":"M Bucher","year":"2016","unstructured":"Bucher M, Wolfowicz I, Voss PA, Hambleton EA, Guse A. Development and symbiosis establishment in the cnidarian endosymbiosis model Aiptasia sp. Sci Rep. 2016;6:19867.","journal-title":"Sci Rep"},{"key":"243_CR7","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1002\/jmor.1051600303","volume":"160","author":"F-S Chia","year":"1979","unstructured":"Chia F-S, Koss R. Fine structural studies of the nervous system and the apical organ in the planula larva of the sea anemone Anthopleura elegantissima. J Morphol. 1979;160:275\u201397.","journal-title":"J Morphol"},{"key":"243_CR8","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/0022-0981(89)90206-2","volume":"127","author":"F-S Chia","year":"1989","unstructured":"Chia F-S, L\u00fctzen J, Svane I. Sexual reproduction and larval morphology of the primitive anthozoan Gonactinia prolifera M. Sars. J Exp Mar Biol Ecol. 1989;127:13\u201324.","journal-title":"J Exp Mar Biol Ecol"},{"key":"243_CR9","doi-asserted-by":"publisher","first-page":"5235","DOI":"10.1073\/pnas.1722151115","volume":"115","author":"PA Cleves","year":"2018","unstructured":"Cleves PA, Strader ME, Bay LK, Pringle JR, Matz MV. CRISPR\/Cas9-mediated genome editing in a reef-building coral. Proc Natl Acad Sci. 2018;115:5235\u201340.","journal-title":"Proc Natl Acad Sci"},{"key":"243_CR10","doi-asserted-by":"publisher","first-page":"3484","DOI":"10.1016\/j.cub.2020.06.099","volume":"30","author":"K Crawford","year":"2020","unstructured":"Crawford K, Diaz Quiroz JF, Koenig KM, Ahuja N, Albertin CB, Rosenthal JJC. Highly efficient knockout of a squid pigmentation gene. Curr Biol CB. 2020;30:3484-3490.e4.","journal-title":"Curr Biol CB"},{"key":"243_CR11","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1016\/j.tig.2008.07.001","volume":"24","author":"CN David","year":"2008","unstructured":"David CN, \u00d6zbek S, Adamczyk P, Meier S, Pauly B, Chapman J, Hwang JS, Gojobori T, Holstein TW. Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet. 2008;24:431\u20138.","journal-title":"Trends Genet"},{"key":"243_CR12","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1007\/s00338-012-0983-z","volume":"32","author":"J Dimond","year":"2013","unstructured":"Dimond J, Kerwin A, Rotjan R, Sharp K, Stewart F, Thornhill D. A simple temperature-based model predicts the upper latitudinal limit of the temperate coral Astrangia poculata. Coral Reefs. 2013;32:401\u20139.","journal-title":"Coral Reefs"},{"key":"243_CR13","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1126\/science.aay6782","volume":"367","author":"TQ DuBuc","year":"2020","unstructured":"DuBuc TQ, Schnitzler CE, Chrysostomou E, McMahon ET, Febrimarsa, Gahan JM, Buggie T, Gornik SG, HanleyBarreira SSN, et al. Transcription factor AP2 controls cnidarian germ cell induction. Science. 2020;367:757\u201362.","journal-title":"Science"},{"key":"243_CR14","doi-asserted-by":"publisher","first-page":"3057","DOI":"10.1242\/dev.046631","volume":"137","author":"DJ Duffy","year":"2010","unstructured":"Duffy DJ, Plickert G, Kuenzel T, Tilmann W, Frank U. Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration. Development. 2010;137:3057\u201366.","journal-title":"Development"},{"key":"243_CR15","doi-asserted-by":"publisher","first-page":"250","DOI":"10.2307\/25066607","volume":"212","author":"SR Dunn","year":"2007","unstructured":"Dunn SR, Phillips WS, Green DR, Weis VM. Knockdown of actin and caspase gene expression by RNA interference in the symbiotic anemone Aiptasia pallida. Biol Bull. 2007;212:250\u20138.","journal-title":"Biol Bull"},{"key":"243_CR16","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1080\/23802359.2022.2079100","volume":"7","author":"X Fang","year":"2022","unstructured":"Fang X, Zhou K, Chen J. The complete linear mitochondrial genome of the hydrozoan jellyfish Cladonema multiramosum Zhou et al., 2022 (Cnidaria: Hydrozoa: Cladonematidae). Mitochondrial DNA Part B Resour. 2022;7:921\u20133.","journal-title":"Mitochondrial DNA Part B Resour"},{"key":"243_CR17","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1016\/j.ydbio.2007.07.029","volume":"310","author":"JH Fritzenwanker","year":"2007","unstructured":"Fritzenwanker JH, Genikhovich G, Kraus Y, Technau U. Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol. 2007;310:264\u201379.","journal-title":"Dev Biol"},{"key":"243_CR18","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1016\/j.ydbio.2017.06.006","volume":"428","author":"JM Gahan","year":"2017","unstructured":"Gahan JM, Schnitzler CE, DuBuc TQ, Doonan LB, Kanska J, Gornik SG, Barreira S, Thompson K, Schiffer P, Baxevanis AD, et al. Functional studies on the role of Notch signaling in Hydractinia development. Dev Biol. 2017;428:224\u201331.","journal-title":"Dev Biol"},{"key":"243_CR19","first-page":"dev200833","volume":"149","author":"E Gilbert","year":"2022","unstructured":"Gilbert E, Teeling C, Lebedeva T, Pedersen S, Chrismas N, Genikhovich G, Modepalli V. Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis. Dev Camb Engl. 2022;149:dev200833.","journal-title":"Dev Camb Engl"},{"key":"243_CR20","doi-asserted-by":"publisher","first-page":"644","DOI":"10.1038\/nbt.1883","volume":"29","author":"MG Grabherr","year":"2011","unstructured":"Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644\u201352.","journal-title":"Nat Biotechnol"},{"key":"243_CR21","doi-asserted-by":"publisher","first-page":"169","DOI":"10.2307\/1542110","volume":"182","author":"C Hand","year":"1992","unstructured":"Hand C, Uhlinger KR. The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull. 1992;182:169\u201376.","journal-title":"Biol Bull"},{"key":"243_CR22","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/j.ydbio.2015.01.006","volume":"399","author":"DC Hayward","year":"2015","unstructured":"Hayward DC, Grasso LC, Saint R, Miller DJ, Ball EE. The organizer in evolution\u2013gastrulation and organizer gene expression highlight the importance of Brachyury during development of the coral, Acropora millepora. Dev Biol. 2015;399:337\u201347.","journal-title":"Dev Biol"},{"key":"243_CR23","doi-asserted-by":"publisher","first-page":"1377","DOI":"10.1126\/science.aar8384","volume":"361","author":"S He","year":"2018","unstructured":"He S, del Viso F, Chen C-Y, Ikmi A, Kroesen AE, Gibson MC. An axial Hox code controls tissue segmentation and body patterning in Nematostella vectensis. Science. 2018;361:1377\u201380.","journal-title":"Science"},{"key":"243_CR24","doi-asserted-by":"publisher","first-page":"5486","DOI":"10.1038\/ncomms6486","volume":"5","author":"A Ikmi","year":"2014","unstructured":"Ikmi A, McKinney SA, Delventhal KM, Gibson MC. TALEN and CRISPR\/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis. Nat Commun. 2014;5:5486.","journal-title":"Nat Commun"},{"key":"243_CR25","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.ydbio.2019.01.005","volume":"448","author":"A Karabulut","year":"2019","unstructured":"Karabulut A, He S, Chen C-Y, McKinney SA, Gibson MC. Electroporation of short hairpin RNAs for rapid and efficient gene knockdown in the starlet sea anemone, Nematostella vectensis. Dev Biol. 2019;448:7\u201315.","journal-title":"Dev Biol"},{"key":"243_CR26","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1186\/s12862-018-1142-0","volume":"18","author":"E Kayal","year":"2018","unstructured":"Kayal E, Bentlage B, Sabrina Pankey M, Ohdera AH, Medina M, Plachetzki DC, Collins AG, Ryan JF. Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits. BMC Evol Biol. 2018;18:68.","journal-title":"BMC Evol Biol"},{"key":"243_CR27","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0011490","volume":"5","author":"MV Kitahara","year":"2010","unstructured":"Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ. A Comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS ONE. 2010;5: e11490.","journal-title":"PLoS ONE"},{"key":"243_CR28","doi-asserted-by":"publisher","first-page":"W171","DOI":"10.1093\/nar\/gkz365","volume":"47","author":"K Labun","year":"2019","unstructured":"Labun K, Montague TG, Krause M, Torres Cleuren YN, Tjeldnes H, Valen E. CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing. Nucleic Acids Res. 2019;47:W171\u20134.","journal-title":"Nucleic Acids Res"},{"key":"243_CR29","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"9","author":"B Langmead","year":"2012","unstructured":"Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357\u20139.","journal-title":"Nat Methods"},{"key":"243_CR30","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0102222","volume":"9","author":"AI Larsson","year":"2014","unstructured":"Larsson AI, J\u00e4rnegren J, Str\u00f6mberg SM, Dahl MP, Lund\u00e4lv T, Brooke S. Embryogenesis and larval biology of the cold-water coral Lophelia pertusa. PLoS ONE. 2014;9: e102222.","journal-title":"PLoS ONE"},{"key":"243_CR31","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1038\/nprot.2013.009","volume":"8","author":"MJ Layden","year":"2013","unstructured":"Layden MJ, R\u00f6ttinger E, Wolenski FS, Gilmore TD, Martindale MQ. Microinjection of mRNA or morpholinos for reverse genetic analysis in the starlet sea anemone, Nematostella vectensis. Nat Protoc. 2013;8:924\u201334.","journal-title":"Nat Protoc"},{"key":"243_CR32","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1002\/wdev.222","volume":"5","author":"MJ Layden","year":"2016","unstructured":"Layden MJ, Rentzsch F, R\u00f6ttinger E. The rise of the starlet sea anemone Nematostella vectensis as a model system to investigate development and regeneration: Overview of starlet sea anemone Nematostella vectensis. Wiley Interdiscip Rev Dev Biol. 2016;5:408\u201328.","journal-title":"Wiley Interdiscip Rev Dev Biol"},{"key":"243_CR33","doi-asserted-by":"publisher","first-page":"2476","DOI":"10.1038\/s41467-025-57109-w","volume":"16","author":"T Lebedeva","year":"2025","unstructured":"Lebedeva T, Bostr\u00f6m J, Kremnyov S, M\u00f6rsdorf D, Niedermoser I, Genikhovich E, Hejnol A, Adameyko I, Genikhovich G. \u03b2-catenin-driven endomesoderm specification is a Bilateria-specific novelty. Nat Commun. 2025;16:2476.","journal-title":"Nat Commun"},{"key":"243_CR34","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1006\/dbio.1999.9407","volume":"214","author":"JU Lohmann","year":"1999","unstructured":"Lohmann JU, Endl I, Bosch TC. Silencing of developmental genes in Hydra. Dev Biol. 1999;214:211\u20134.","journal-title":"Dev Biol"},{"key":"243_CR35","doi-asserted-by":"publisher","first-page":"10","DOI":"10.14806\/ej.17.1.200","volume":"17","author":"M Martin","year":"2011","unstructured":"Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10.","journal-title":"EMBnet J"},{"key":"243_CR36","doi-asserted-by":"publisher","first-page":"16049","DOI":"10.1038\/s41598-022-20476-1","volume":"12","author":"T Masuda-Ozawa","year":"2022","unstructured":"Masuda-Ozawa T, Fujita S, Nakamura R, Watanabe H, Kuranaga E, Nakajima Y. siRNA-mediated gene knockdown via electroporation in hydrozoan jellyfish embryos. Sci Rep. 2022;12:16049.","journal-title":"Sci Rep"},{"key":"243_CR37","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/s00427-006-0122-3","volume":"217","author":"DQ Matus","year":"2007","unstructured":"Matus DQ, Thomsen GH, Martindale MQ. FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. Dev Genes Evol. 2007;217:137\u201348.","journal-title":"Dev Genes Evol"},{"key":"243_CR38","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1093\/sysbio\/syaa103","volume":"70","author":"CS McFadden","year":"2021","unstructured":"McFadden CS, Quattrini AM, Brugler MR, Cowman PF, Due\u00f1as LF, Kitahara MV, Paz-Garc\u00eda DA, Reimer JD, Rodr\u00edguez E. Phylogenomics, origin, and diversification of anthozoans (Phylum Cnidaria). Syst Biol. 2021;70:635\u201347.","journal-title":"Syst Biol"},{"key":"243_CR39","doi-asserted-by":"publisher","first-page":"11734","DOI":"10.1038\/s41598-018-30188-0","volume":"8","author":"T Momose","year":"2018","unstructured":"Momose T, De Cian A, Shiba K, Inaba K, Giovannangeli C, Concordet J-P. High doses of CRISPR\/Cas9 ribonucleoprotein efficiently induce gene knockout with low mosaicism in the hydrozoan Clytia hemisphaerica through microhomology-mediated deletion. Sci Rep. 2018;8:11734.","journal-title":"Sci Rep"},{"key":"243_CR40","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.ydbio.2022.07.008","volume":"490","author":"N Oulhen","year":"2022","unstructured":"Oulhen N, Pieplow C, Perillo M, Gregory P, Wessel GM. Optimizing CRISPR\/Cas9-based gene manipulation in echinoderms. Dev Biol. 2022;490:117\u201324.","journal-title":"Dev Biol"},{"key":"243_CR41","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2215958120","volume":"120","author":"A Paix","year":"2023","unstructured":"Paix A, Basu S, Steenbergen P, Singh R, Prevedel R, Ikmi A. Endogenous tagging of multiple cellular components in the sea anemone Nematostella vectensis. Proc Natl Acad Sci. 2023;120: e2215958120.","journal-title":"Proc Natl Acad Sci"},{"key":"243_CR42","first-page":"199771","volume":"148","author":"JS Presnell","year":"2021","unstructured":"Presnell JS, Browne WE. Kr\u00fcppel-like factor gene function in the ctenophore Mnemiopsis leidyi assessed by CRISPR\/Cas9-mediated genome editing. Dev Camb Engl. 2021;148:199771.","journal-title":"Dev. Camb. Engl."},{"key":"243_CR43","doi-asserted-by":"publisher","DOI":"10.1128\/mmbr.00053-22","volume":"86","author":"G Puntin","year":"2022","unstructured":"Puntin G, Sweet M, Fraune S, Medina M, Sharp K, Weis VM, Ziegler M. Harnessing the power of model organisms to unravel microbial functions in the coral holobiont. Microbiol Mol Biol Rev MMBR. 2022;86: e0005322.","journal-title":"Microbiol Mol Biol Rev MMBR"},{"key":"243_CR44","doi-asserted-by":"publisher","first-page":"D590","DOI":"10.1093\/nar\/gks1219","volume":"41","author":"C Quast","year":"2013","unstructured":"Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Gl\u00f6ckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590\u20136.","journal-title":"Nucleic Acids Res"},{"key":"243_CR45","doi-asserted-by":"publisher","first-page":"e29555","DOI":"10.7554\/eLife.29555","volume":"7","author":"G Quiroga Artigas","year":"2018","unstructured":"Quiroga Artigas G, Lap\u00e9bie P, Lecl\u00e8re L, Takeda N, Deguchi R, J\u00e9kely G, Momose T, Houliston E. A gonad-expressed opsin mediates light-induced spawning in the jellyfish Clytia. Elife. 2018;7:e29555.","journal-title":"Elife"},{"key":"243_CR46","doi-asserted-by":"publisher","first-page":"12806","DOI":"10.1038\/s41598-020-69489-8","volume":"10","author":"G Quiroga-Artigas","year":"2020","unstructured":"Quiroga-Artigas G, Duscher A, Lundquist K, Waletich J, Schnitzler CE. Gene knockdown via electroporation of short hairpin RNAs in embryos of the marine hydroid Hydractinia symbiolongicarpus. Sci Rep. 2020;10:12806.","journal-title":"Sci Rep"},{"key":"243_CR47","unstructured":"R Core Team. 2020. R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna Austria."},{"key":"243_CR48","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.1242\/dev.020784","volume":"135","author":"F Rentzsch","year":"2008","unstructured":"Rentzsch F, Fritzenwanker JH, Scholz CB, Technau U. FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development. 2008;135:1761\u20139.","journal-title":"Development"},{"key":"243_CR49","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003164","volume":"8","author":"E R\u00f6ttinger","year":"2012","unstructured":"R\u00f6ttinger E, Dahlin P, Martindale MQ. A framework for the establishment of a cnidarian gene regulatory network for \u201cendomesoderm\u201d specification: The inputs of \u00df-Catenin\/TCF signaling. PLoS Genet. 2012;8: e1003164.","journal-title":"PLoS Genet"},{"key":"243_CR50","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1186\/s12864-018-5032-z","volume":"19","author":"SM Sanders","year":"2018","unstructured":"Sanders SM, Ma Z, Hughes JM, Riscoe BM, Gibson GA, Watson AM, Flici H, Frank U, Schnitzler CE, Baxevanis AD, et al. CRISPR\/Cas9-mediated gene knockin in the hydroid Hydractinia symbiolongicarpus. BMC Genomics. 2018;19:649.","journal-title":"BMC Genomics"},{"key":"243_CR51","doi-asserted-by":"publisher","first-page":"222","DOI":"10.15517\/rev.biol.trop..v70i1.48648","volume":"70","author":"J-D Santiago-Valent\u00edn","year":"2022","unstructured":"Santiago-Valent\u00edn J-D, Rodr\u00edguez-Troncoso A-P, Bautista-Guerrero E, L\u00f3pez-P\u00e9rez A, Cupul-Maga\u00f1a A-L, Santiago-Valent\u00edn J-D, Rodr\u00edguez-Troncoso A-P, Bautista-Guerrero E, L\u00f3pez-P\u00e9rez A, Cupul-Maga\u00f1a A-L. Internal ultrastructure of the planktonic larva of the coral Porites panamensis (Anthozoa: Scleractinia). Rev Biol Trop. 2022;70:222\u201334.","journal-title":"Rev Biol Trop"},{"key":"243_CR52","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","volume":"9","author":"J Schindelin","year":"2012","unstructured":"Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676\u201382.","journal-title":"Nat Methods"},{"key":"243_CR53","doi-asserted-by":"publisher","first-page":"e75050","DOI":"10.7554\/eLife.75050","volume":"10","author":"A Seleit","year":"2021","unstructured":"Seleit A, Aulehla A, Paix A. Endogenous protein tagging in medaka using a simplified CRISPR\/Cas9 knock-in approach. Elife. 2021;10:e75050.","journal-title":"Elife"},{"key":"243_CR54","doi-asserted-by":"publisher","first-page":"2951","DOI":"10.1242\/dev.145839","volume":"144","author":"MD Servetnick","year":"2017","unstructured":"Servetnick MD, Steinworth B, Babonis LS, Simmons D, Salinas-Saavedra M, Martindale MQ. Cas9-mediated excision of Nematostella brachyury disrupts endoderm development, pharynx formation, and oral\u2013aboral patterning. Development. 2017;144:2951\u201360.","journal-title":"Development"},{"key":"243_CR55","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1016\/j.ydbio.2014.11.019","volume":"398","author":"C Sinigaglia","year":"2015","unstructured":"Sinigaglia C, Busengdal H, Lerner A, Oliveri P, Rentzsch F. Molecular characterization of the apical organ of the anthozoan Nematostella vectensis. Dev Biol. 2015;398:120\u201333.","journal-title":"Dev Biol"},{"key":"243_CR56","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1186\/s13742-015-0089-y","volume":"4","author":"L Song","year":"2015","unstructured":"Song L, Florea L. Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads. GigaScience. 2015;4:48.","journal-title":"GigaScience"},{"key":"243_CR57","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1186\/s12864-017-4392-0","volume":"19","author":"ME Strader","year":"2018","unstructured":"Strader ME, Aglyamova GV, Matz MV. Molecular characterization of larval development from fertilization to metamorphosis in a reef-building coral. BMC Genomics. 2018;19:17.","journal-title":"BMC Genomics"},{"key":"243_CR58","doi-asserted-by":"publisher","first-page":"257","DOI":"10.2307\/1540935","volume":"158","author":"A Szmant-Froelich","year":"1980","unstructured":"Szmant-Froelich A, Yevich P, Pilson MEQ. Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol Bull. 1980;158:257\u201369.","journal-title":"Biol Bull"},{"key":"243_CR59","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2216144120","volume":"120","author":"AI Tinoco","year":"2023","unstructured":"Tinoco AI, Mitchison-Field LMY, Bradford J, Renicke C, Perrin D, Bay LK, Pringle JR, Cleves PA. Role of the bicarbonate transporter SLC4\u03b3 in stony-coral skeleton formation and evolution. Proc Natl Acad Sci. 2023;120: e2216144120.","journal-title":"Proc Natl Acad Sci"},{"key":"243_CR60","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1111\/ivb.12025","volume":"132","author":"C Tran","year":"2013","unstructured":"Tran C, Hadfield MG. Localization of sensory mechanisms utilized by coral planulae to detect settlement cues. Invertebr Biol. 2013;132:195\u2013206.","journal-title":"Invertebr Biol"},{"key":"243_CR61","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1017\/S0025315400070387","volume":"62","author":"PRG Tranter","year":"1982","unstructured":"Tranter PRG, Nicholson DN, Kinchington D. A description of spawning and post-gastrula development of the cool temperate coral, Caryophyllia Smithi. J Mar Biol Assoc U K. 1982;62:845\u201354.","journal-title":"J Mar Biol Assoc U K"},{"key":"243_CR62","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1038\/nprot.2013.014","volume":"8","author":"FS Wolenski","year":"2013","unstructured":"Wolenski FS, Layden MJ, Martindale MQ, Gilmore TD, Finnerty JR. Characterizing the spatiotemporal expression of RNAs and proteins in the starlet sea anemone, Nematostella vectensis. Nat Protoc. 2013;8:900\u201315.","journal-title":"Nat Protoc"},{"key":"243_CR63","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmars.2021.688876","volume":"2","author":"I Yuyama","year":"2021","unstructured":"Yuyama I, Higuchi T, Hidaka M. Application of RNA interference technology to acroporid juvenile corals. Front Mar Sci. 2021;2:1\u20139. https:\/\/doi.org\/10.3389\/fmars.2021.688876.","journal-title":"Front Mar Sci"},{"key":"243_CR64","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0022725","volume":"6","author":"C Zenkert","year":"2011","unstructured":"Zenkert C, Takahashi T, Diesner M-O, \u00d6zbek S. Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS ONE. 2011;6: e22725.","journal-title":"PLoS ONE"}],"container-title":["EvoDevo"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13227-025-00243-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13227-025-00243-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13227-025-00243-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T10:03:27Z","timestamp":1747389807000},"score":1,"resource":{"primary":{"URL":"https:\/\/evodevojournal.biomedcentral.com\/articles\/10.1186\/s13227-025-00243-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,16]]},"references-count":64,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["243"],"URL":"https:\/\/doi.org\/10.1186\/s13227-025-00243-9","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.11.16.567385","asserted-by":"object"}]},"ISSN":["2041-9139"],"issn-type":[{"value":"2041-9139","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,16]]},"assertion":[{"value":"19 March 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 May 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 May 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"6"}}