دورية أكاديمية
Genetic tools for the study of the mangrove killifish, Kryptolebias marmoratus, an emerging vertebrate model for phenotypic plasticity.
| العنوان: | Genetic tools for the study of the mangrove killifish, Kryptolebias marmoratus, an emerging vertebrate model for phenotypic plasticity. |
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| المؤلفون: | Li CY; Department of Biology, University of Maryland, College Park, Maryland, USA., Boldt H; Department of Genetics, Harvard Medical School, Boston, Massachusetts, USA.; Department of Orthopaedic Surgery, Boston Children's Hospital, Boston, Massachusetts, USA., Parent E; Department of Biology, University of Maryland, College Park, Maryland, USA., Ficklin J; Department of Biology, University of Maryland, College Park, Maryland, USA.; College of Computer, Mathematical, and Natural Sciences, Biological Sciences Graduate Program, University of Maryland, College Park, Maryland, USA., James A; Department of Orthopaedic Surgery, Boston Children's Hospital, Boston, Massachusetts, USA., Anlage TJ; Department of Biology, University of Maryland, College Park, Maryland, USA., Boyer LM; Department of Biology, University of Maryland, College Park, Maryland, USA., Pierce BR; Department of Biology, University of Maryland, College Park, Maryland, USA., Siegfried KR; Department of Biology, University of Massachusetts, Boston, Massachusetts, USA., Harris MP; Department of Genetics, Harvard Medical School, Boston, Massachusetts, USA.; Department of Orthopaedic Surgery, Boston Children's Hospital, Boston, Massachusetts, USA., Haag ES; Department of Biology, University of Maryland, College Park, Maryland, USA. |
| المصدر: | Journal of experimental zoology. Part B, Molecular and developmental evolution [J Exp Zool B Mol Dev Evol] 2024 May; Vol. 342 (3), pp. 164-177. Date of Electronic Publication: 2023 Aug 08. |
| نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.; Research Support, N.I.H., Extramural |
| اللغة: | English |
| بيانات الدورية: | Publisher: Wiley-Liss Country of Publication: United States NLM ID: 101168228 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1552-5015 (Electronic) Linking ISSN: 15525007 NLM ISO Abbreviation: J Exp Zool B Mol Dev Evol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Hoboken, NJ : Wiley-Liss, c2003- |
| مواضيع طبية MeSH: | Phenotype*, Animals ; Cyprinodontiformes/genetics ; Cyprinodontiformes/physiology ; Killifishes/genetics ; Killifishes/physiology ; Fundulidae/genetics ; Fundulidae/embryology ; Fundulidae/physiology ; Embryo, Nonmammalian |
| مستخلص: | Kryptolebias marmoratus (Kmar), a teleost fish of the order Cyprinodontiformes, has a suite of unique phenotypes and behaviors not observed in other fishes. Many of these phenotypes are discrete and highly plastic-varying over time within an individual, and in some cases reversible. Kmar and its interfertile sister species, K. hermaphroditus, are the only known self-fertile vertebrates. This unusual sexual mode has the potential to provide unique insights into the regulation of vertebrate sexual development, and also lends itself to genetics. Kmar is easily adapted to the lab and requires little maintenance. However, its internal fertilization and small clutch size limits its experimental use. To support Kmar as a genetic model, we compared alternative husbandry techniques to maximize recovery of early cleavage-stage embryos. We find that frequent egg collection enhances yield, and that protease treatment promotes the greatest hatching success. We completed a forward mutagenesis screen and recovered several mutant lines that serve as important tools for genetics in this model. Several will serve as useful viable recessive markers for marking crosses. Importantly, the mutant kissylips lays embryos at twice the rate of wild-type. Combining frequent egg collection with the kissylips mutant background allows for a substantial enhancement of early embryo yield. These improvements were sufficient to allow experimental analysis of early development and the successful mono- and bi-allelic targeted knockout of an endogenous tyrosinase gene with CRISPR/Cas9 nucleases. Collectively, these tools will facilitate modern developmental genetics in this fascinating fish, leading to future insights into the regulation of plasticity. (© 2023 The Authors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution published by Wiley Periodicals LLC.) |
| References: | Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2. Bento, G., Ogawa, A., & Sommer, R. J. (2010). Co‐option of the hormone‐signalling module dafachronic acid‐DAF‐12 in nematode evolution. Nature, 466(7305), 494–497. https://doi.org/10.1038/nature09164. Berbel‐Filho, W. M., Pacheco, G., Tatarenkov, A., Lira, M. G., Garcia de Leaniz, C., Rodríguez López, C. M., Lima, S. M. Q., & Consuegra, S. (2022). Phylogenomics reveals extensive introgression and a case of mito‐nuclear discordance in the killifish genus Kryptolebias. Molecular Phylogenetics and Evolution, 177, 107617. https://doi.org/10.1016/j.ympev.2022.107617. Bertozzi, T. M., & Ferguson‐Smith, A. C. (2020). Metastable epialleles and their contribution to epigenetic inheritance in mammals. Seminars in Cell & Developmental Biology, 97, 93–105. https://doi.org/10.1016/j.semcdb.2019.08.002. Bolker, J. A. (1995). Model systems in developmental biology. BioEssays, 17(5), 451–455. Brinkman, E. K., Chen, T., Amendola, M., & van Steensel, B. (2014). Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Research, 42(22), e168. https://doi.org/10.1093/nar/gku936. Bui, L. T., Ivers, N. A., & Ragsdale, E. J. (2018). A sulfotransferase dosage‐dependently regulates mouthpart polyphenism in the nematode Pristionchus pacificus. Nature Communications, 9(1), 4119. https://doi.org/10.1038/s41467-018-05612-8. Chey, M., & Jose, A. M. (2022). Heritable epigenetic changes at single genes: challenges and opportunities in Caenorhabditis elegans. Trends in Genetics, 38(2), 116–119. https://doi.org/10.1016/j.tig.2021.08.011. Driever, W., Solnica‐Krezel, L., Schier, A. F., Neuhauss, S. C. F., Malicki, J., Stemple, D. L., Stainier, D. Y. R., Zwartkruis, F., Abdelilah, S., Rangini, Z., Belak, J., & Boggs, C. (1996). A genetic screen for mutations affecting embryogenesis in zebrafish. Development, 123(1), 37–46. https://doi.org/10.1242/dev.123.1.37. Earley, R. L., Hanninen, A. F., Fuller, A., Garcia, M. J., & Lee, E. A. (2012). Phenotypic plasticity and integration in the mangrove rivulus (Kryptolebias marmoratus): A prospectus. Integrative and Comparative Biology, 52(6), 814–827. https://doi.org/10.1093/icb/ics118. Edenbrow, M., & Croft, D. P. (2013). Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus. Oikos, 122(5), 667–681. https://doi.org/10.1111/j.1600-0706.2012.20556.x. Fielenbach, N., & Antebi, A. (2008). C. elegans dauer formation and the molecular basis of plasticity. Genes & Development, 22(16), 2149–2165. https://doi.org/10.1101/gad.1701508. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J. J. M., van Eeden, F., Jiang, Y.‐J., Heisenberg, C.‐P., Kelsh, R. N., Furutani‐Seiki, M., Vogelsang, E., Beuchle, D., Schach, U., Fabian, C., & Nüsslein‐Volhard, C. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development, 123(1), 1–36. https://doi.org/10.1242/dev.123.1.1. Harrington, R. (1967). Environmentally controlled induction of primary males gonochorists from eggs of the self‐fertilizaing hermaphroditic fish, Rivulus marmoratus Poey. Biological Bulletin, 131, 174–199. Harrington, Jr., R. W. (1961). Oviparous hermaphroditic fish with internal self‐fertilization. Science, 134(3492), 1749–1750. https://doi.org/10.1126/science.134.3492.1749. Harrington, Jr., R. W. (1963). Twenty‐four‐hour rhythms of internal self‐fertilization and of oviposition by hermaphrodites of Rivulus marmoratus. Physiological Zoology, 36(4), 325–341. Harrington, Jr., R. W., & Kallman, K. D. (1968). The homozygosity of clones of the self‐fertilizing hermaphroditic fish Rivulus marmoratus Poey (Cyprinodontidae, Atheriniformes). The American Naturalist, 102(926), 337–343. Harrington, Jr., R. W., & Rivas, L. R. (1958). The discovery in Florida of the cyprinodont fish, Rivulus marmoratus, with a redescription and ecological notes. Copeia, 1958(2), 125–130. Heffell, Q., Turko, A. J., & Wright, P. A. (2018). Plasticity of skin water permeability and skin thickness in the amphibious mangrove rivulus Kryptolebias marmoratus. Journal of Comparative Physiology B, 188(2), 305–314. https://doi.org/10.1007/s00360-017-1123-4. Hoshijima, K., Jurynec, M. J., Klatt Shaw, D., Jacobi, A. M., Behlke, M. A., & Grunwald, D. J. (2019). Highly efficient CRISPR‐Cas9‐based methods for generating deletion mutations and F0 embryos that lack gene function in zebrafish. Developmental Cell, 51(5), 645–657. https://doi.org/10.1016/j.devcel.2019.10.004. Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J. C., Koch, R., Rauch, G. J., White, S., … Teucke, M. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature, 496(7446), 498–503. https://doi.org/10.1038/nature12111. Hsu, Y., & Wolf, L. L. (1999). The winner and loser effect: integrating multiple experiences. Animal Behaviour, 57(4), 903–910. https://doi.org/10.1006/anbe.1998.1049. Huehner, M. K., Schramm, M. E., & Hens, M. D. (1985). Notes on the behavior and ecology of the killifish Rivulus marmoratus poey 1880 (Cyprinodontidae). Florida Scient. 48(1), 1–7. Retrieved from: http://www.jstor.org.proxy-um.researchport.umd.edu/stable/24319873. Kanamori, A., Sugita, Y., Yuasa, Y., Suzuki, T., Kawamura, K., Uno, Y., Kamimura, K., Matsuda, Y., Wilson, C. A., Amores, A., Postlethwait, J. H., Suga, K., & Sakakura, Y. (2016). A genetic map for the only self‐fertilizing vertebrate. G3: Genes|Genomes|Genetics, 6(4), 1095–1106. https://doi.org/10.1534/g3.115.022699. Kanamori, A., Yamamura, A., Koshiba, S., Lee, J. S., Orlando, E. F., & Hori, H. (2006). Methyltestosterone efficiently induces male development in the self‐fertilizing hermaphrodite fish, Kryptolebias marmoratus. Genesis, 44(10), 495–503. https://doi.org/10.1002/dvg.20240. Kasahara, M., Naruse, K., Sasaki, S., Nakatani, Y., Qu, W., Ahsan, B., Yamada, T., Nagayasu, Y., Doi, K., Kasai, Y., Jindo, T., Kobayashi, D., Shimada, A., Toyoda, A., Kuroki, Y., Fujiyama, A., Sasaki, T., Shimizu, A., Asakawa, S., … Kohara, Y. (2007). The medaka draft genome and insights into vertebrate genome evolution. Nature, 447(7145), 714–719. https://doi.org/10.1038/nature05846. Kelley, J. L., Yee, M. C., Brown, A. P., Richardson, R. R., Tatarenkov, A., Lee, C. C., Harkins, T. T., Bustamante, C. D., & Earley, R. L. (2016). The genome of the self‐fertilizing mangrove rivulus fish, Kryptolebias marmoratus: A model for studying phenotypic plasticity and adaptations to extreme environments. Genome Biology and Evolution, 8, 2145–2154. https://doi.org/10.1093/gbe/evw145. King, J. A. C., Abel, D. C., & DiBona, D. R. (1989). Effects of salinity on chloride cells in the euryhaline cyprinodontid fish Rivulus marmoratus. Cell and Tissue Research, 257(2), 367–377. https://doi.org/10.1007/BF00261839. Leblanc, D. M., Wood, C. M., Fudge, D. S., & Wright, P. A. (2010). A fish out of water: Gill and skin remodeling promotes osmo‐ and ionoregulation in the mangrove killifish Kryptolebias marmoratus. Physiological and Biochemical Zoology, 83(6), 932–949. https://doi.org/10.1086/656307. Li, C. Y., Steighner, J. R., Sweatt, G., Thiele, T. R., & Juntti, S. A. (2021). Manipulation of the Tyrosinase gene permits improved CRISPR/Cas editing and neural imaging in cichlid fish. Scientific Reports, 11(1), 15138. https://doi.org/10.1038/s41598-021-94577-8. Lomax, J. L., Carlson, R. E., Wells, J. W., Crawford, P. M., & Earley, R. L. (2017). Factors affecting egg production in the selfing mangrove rivulus (Kryptolebias marmoratus). Zoology, 122, 38–45. https://doi.org/10.1016/j.zool.2017.02.004. Loosli, F., Köster, R. W., Carl, M., Kühnlein, R., Henrich, T., Mücke, M., Krone, A., & Wittbrodt, J. (2000). A genetic screen for mutations affecting embryonic development in medaka fish (Oryzias latipes). Mechanisms of Development, 97(1–2), 133–139. https://doi.org/10.1016/s0925‐4773(00)00406‐8. Lubinski, B. A., Davis, W. P., Taylor, D. S., & Turner, B. J. (1995). Outcrossing in a natural population of a self‐fertilizing hermaphroditic fish. Journal of Heredity, 86, 469–473. Mackiewicz, M., Tatarenkov, A., Perry, A., Martin, J. R., Elder, Jr., J. F., Bechler, D. L., & Avise, J. C. (2006a). Microsatellite documentation of male‐mediated outcrossing between inbred laboratory strains of the self‐fertilizing mangrove killifish (Kryptolebias marmoratus). Journal of Heredity, 97(5), 508–513. https://doi.org/10.1093/jhered/esl017. Mackiewicz, M., Tatarenkov, A., Taylor, D. S., Turner, B. J., & Avise, J. C. (2006b). Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self‐fertilizing hermaphrodite. Proceedings of the National Academy of Sciences, 103(26), 9924–9928. https://doi.org/10.1073/pnas.0603847103. Mackiewicz, M., Tatarenkov, A., Turner, B. J., & Avise, J. C. (2006c). A mixed‐mating strategy in a hermaphroditic vertebrate. Proceedings. Biological Sciences, 273(1600), 2449–2452. https://doi.org/10.1098/rspb.2006.3594. McCain, S. C., Kopelic, S., Houslay, T. M., Wilson, A. J., Lu, H., & Earley, R. L. (2020). Choice consequences: Salinity preferences and hatchling survival in the mangrove rivulus (Kryptolebias marmoratus). The Journal of Experimental Biology, 223(Pt 5), jeb219196. https://doi.org/10.1242/jeb.219196. Mesak, F., Tatarenkov, A., & Avise, J. C. (2015). Transcriptomics of diapause in an isogenic self‐fertilizing vertebrate. BMC Genomics, 16, 989. https://doi.org/10.1186/s12864-015-2210-0. Moore, G. L., Sucar, S., Newsome, J. M., Ard, M. E., Bernhardt, L., Bland, M. J., & Ring, B. C. (2012). Establishing developmental genetics in a self‐fertilizing fish (Krytolebias marmoratus). Integrative and comparative biology, 52(6), 781–791. https://doi.org/10.1093/icb/ics052. Mourabit, S., Edenbrow, M., Croft, D. P., & Kudoh, T. (2011). Embryonic development of the self‐fertilizing mangrove killifish Kryptolebias marmoratus. Developmental Dynamics, 240(7), 1694–1704. https://doi.org/10.1002/dvdy.22668. Mourabit, S., & Kudoh, T. (2012). Manipulation and imaging of Kryptolebias marmoratus embryos. Integrative and Comparative Biology, 52(6), 761–768. https://doi.org/10.1093/icb/ics076. Nakamura, Y., Suga, K., Sakakura, Y., Sakamoto, T., & Hagiwara, A. (2008). Genetic and growth differences in the outcrossings between two clonal strains of the self‐fertilizing mangrove killifish. Canadian Journal of Zoology, 86(9), 976–982. https://doi.org/10.1139/z08-075. Ong, K. J., Stevens, E. D., & Wright, P. A. (2007). Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. Journal of Experimental Biology, 210(Pt 7), 1109–1115. https://doi.org/10.1242/jeb.002238. Orlando, E. F. (2012). “Mangrove ‘killifish’: An exemplar of integrative biology”: Introduction to the symposium. Integrative and Comparative Biology, 52(6), 721–723. https://doi.org/10.1093/icb/ics103. Reardon, S. (2019). CRISPR gene‐editing creates wave of exotic model organisms. Nature, 568(7753), 441–442. https://doi.org/10.1038/d41586-019-01300-9. Rohner, N., Perathoner, S., Frohnhöfer, H. G., & Harris, M. P. (2011). Enhancing the efficiency of N‐ethyl‐N‐nitrosourea‐induced mutagenesis in the zebrafish. Zebrafish, 8(3), 119–123. https://doi.org/10.1089/zeb.2011.0703. Rossi, G. S., Cochrane, P. V., & Wright, P. A. (2020). Fluctuating environments during early development can limit adult phenotypic flexibility: insights from an amphibious fish. The Journal of Experimental Biology, 223(Pt 16), jeb228304. https://doi.org/10.1242/jeb.228304. Sakakura, Y., & Noakes, D. L. G. (2000). Age, growth, and sexual development in the self‐fertilizing hermaphroditic fish Rivulus marmoratus. Environmental Biology of Fishes, 59, 309–317. Saud, H. A., O'Neill, P. A., Ono, Y., Verbruggen, B., Van Aerle, R., Kim, J., Lee, J. S., Ring, B. C., & Kudoh, T. (2021). Molecular mechanisms of embryonic tail development in the self‐fertilizing mangrove killifish Kryptolebias marmoratus. Development, 148(24), dev199675. https://doi.org/10.1242/dev.199675. Sieriebriennikov, B., Markov, G. V., Witte, H., & Sommer, R. J. (2017). The role of DAF‐21/Hsp90 in mouth‐form plasticity in Pristionchus pacificus. Molecular Biology and Evolution, 34(7), 1644–1653. https://doi.org/10.1093/molbev/msx106. Sucar, S., Moore, G. L., Ard, M. E., & Ring, B. C. (2016). A simultaneous genetic screen for zygotic and sterile mutants in a hermaphroditic vertebrate (Kryptolebias marmoratus). G3: Genes|Genomes|Genetics, 6(4), 1107–1119. https://doi.org/10.1534/g3.115.022475. Tatarenkov, A., Earley, R. L., Taylor, D. S., & Avise, J. C. (2012). Microevolutionary distribution of isogenicity in a self‐fertilizing fish (Kryptolebias marmoratus) in the Florida Keys. Integrative and Comparative Biology, 52(6), 743–752. https://doi.org/10.1093/icb/ics075. Tatarenkov, A., Earley, R. L., Taylor, D. S., Davis, W. P., & Avise, J. C. (2018). Natural hybridization between divergent lineages in a selfing hermaphroditic fish. Biology Letters, 14(6), 20180118. https://doi.org/10.1098/rsbl.2018.0118. Tatarenkov, A., Gao, H., Mackiewicz, M., Taylor, D. S., Turner, B. J., & Avise, J. C. (2007). Strong population structure despite evidence of recent migration in a selfing hermaphroditic vertebrate, the mangrove killifish (Kryptolebias marmoratus). Molecular Ecology, 16(13), 2701–2711. https://doi.org/10.1111/j.1365-294X.2007.03349.x. Tatarenkov, A., Lima, S. M. Q., Taylor, D. S., & Avise, J. C. (2009). Long‐term retention of self‐fertilization in a fish clade. Proceedings of the National Academy of Sciences, 106(34), 14456–14459. https://doi.org/10.1073/pnas.0907852106. Tatarenkov, A., Ring, B. C., Elder, J. F., Bechler, D. L., & Avise, J. C. (2010). Genetic composition of laboratory stocks of the self‐fertilizing fish Kryptolebias marmoratus: A valuable resource for experimental research. PLoS One, 5(9), e12863. https://doi.org/10.1371/journal.pone.0012863. Taylor, D. S. (2012). Twenty‐four years in the mud: What have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebias marmoratus? Integrative and Comparative Biology, 52(6), 724–736. https://doi.org/10.1093/icb/ics062. Taylor, D. S., Turner, B. J., Davis, W. P., & Chapman, B. B. (2008). A novel terrestrial fish habitat inside emergent logs. The American Naturalist, 171(2), 263–266. https://doi.org/10.1086/524960. Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A., & Warman, M. L. (2000). Preparation of PCR‐quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT. Biotechniques, 29(1), 52–54. https://doi.org/10.2144/00291bm09. Turko, A. J., Cooper, C. A., & Wright, P. A. (2012). Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the amphibious fish Kryptolebias marmoratus. The Journal of Experimental Biology, 215(Pt), 3973–3980. https://doi.org/10.1242/jeb.074831. Turko, A. J., & Rossi, G. S. (2022). Habitat choice promotes and constrains phenotypic plasticity. Biology Letters, 18(1), 20210468. https://doi.org/10.1098/rsbl.2021.0468. Turner, B., Fisher, M., Taylor, D., Davis, W., & Jarrett, B. (2006). Evolution of ‘maleness” and outcrossing in a population of the self‐fertilizing killifish, Kryptolebias marmoratus. Evol. Ecol. Res. 8, 1475–1486. Verdikt, R., Armstrong, A. A., & Allard, P. (2023). Transgenerational inheritance and its modulation by environmental cues. Current Topics in Developmental Biology, 152, 31–76. https://doi.org/10.1016/bs.ctdb.2022.10.002. Wells, M. W., Turko, A. J., & Wright, P. A. (2015). Fish embryos on land: Terrestrial embryo deposition lowers oxygen uptake without altering growth or survival in the amphibious fish Kryptolebias marmoratus. Journal of Experimental Biology, 218(Pt 20), 3249–3256. https://doi.org/10.1242/jeb.127399. Wells, M. W., & Wright, P. A. (2017). Do not eat your kids: Embryonic kin recognition in an amphibious fish. Behavioral Ecology and Sociobiology, 71(10), 140. https://doi.org/10.1007/s00265-017-2360-y. |
| معلومات مُعتمدة: | National Science Foundation |
| فهرسة مساهمة: | Keywords: hermaphroditism; killifish; mutagenesis; plasticity; self‐fertility |
| تواريخ الأحداث: | Date Created: 20230809 Date Completed: 20240430 Latest Revision: 20240430 |
| رمز التحديث: | 20240430 |
| DOI: | 10.1002/jez.b.23216 |
| PMID: | 37553824 |
| قاعدة البيانات: | MEDLINE |
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