Adoption of conserved developmental genes in development and origin of the medusa body plan

EvoDevo - Tập 6 - Trang 1-15 - 2015
Johanna E. M. Kraus1, David Fredman1,2, Wei Wang3, Konstantin Khalturin4, Ulrich Technau1
1Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Wien, Austria
2Present address: Computational Biology Unit, University of Bergen, Bergen, Norway
3Zoologisches Institut, Christian-Albrechts Universität zu Kiel, Kiel, Germany
4Marine Genomics Unit, Okinawa Institute of Science and Technology, Kunigami-gun, Japan

Tóm tắt

The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required. We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen. Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

Tài liệu tham khảo

Wilbur HM. Complex life cycles. Annu Rev Ecol Syst. 1980;11:67–93. Haeckel E. Das system der Medusen: Erster Teil einer Monographie der Medusen, vol. 2. Jena: VEB Gustav Fischer Verlag; 1879. Brooks WK. The life history of the hydromedusae: a discussion of the medusae and of the significance of metagenesis. Mem Boston Soc Nat Hist. 1886;3:359–430. Hadži J. An attempt to reconstruct the system of animal classification. Syst Biol. 1953;2(4):145–54. Salvini‐Plawen LV. On the origin and evolution of the lower Metazoa. J Zool Syst Evol Res. 1978;16(1):40–87. Lv S-P. Mesopsammic cnidaria from plymouth (with systematic notes). J Mar Biol Assoc U K. 1987;67(03):623–37. Korschelt E, Heider K. Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbellosen Tiere, vol. 1. Jena: VEB Gustav Fischer Verlag; 1890. Remane A. Die Geschichte der Tiere. In: Heberer G, editor. Die Evolution der Organismen. 1954. Seipel K, Schmid V. Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol. 2006;50:589–99. Boero F, Gravili C, Pagliara P, Piraino S, Bouillon J, Schmid V. The cnidarian premises of metazoan evolution: from triploblasty, to coelom formation, to metamery. Ital J Zool. 1998;65(1):5–9. Werner B, Cutress CE, Studebaker JP. Life cycle of Tripedalia cystophora Conant (Cubomedusae). Nature. 1971;232(5312):582–3. Stangl K, Salvini-Plawen L, Holstein TW. Staging and induction of medusa metamorphosis in Carybdea marsupialis (Cnidaria, Cubozoa). Vie Milieu. 2002;52(13):1–140. Straehler-Pohl I, Jarms G. Life cycle of Carybdea marsupialis Linnaeus, 1758 (Cubozoa, Carybdeidae) reveals metamorphosis to be a modified strobilation. Mar Biol. 2005;147(6):1271–7. Marques AC, Collins AG. Cladistic analysis of Medusozoa and cnidarian evolution. Invertebr Biol. 2004;123(1):23–42. Kikinger R, Salvini-Plawen L. Development from polyp to stauromedusa in Stylocoronella (Cnidaria: Scyphozoa). JMBA. 1995;75(4):899–912. Huxley TH. The oceanic Hydrozoa; a description of the Calycophoridæ and Physophoridæ observed during the Voyage of HMS “Rattlesnake” in the years 1846–50, with a general introduction, vol. 20. London: Ray Society; 1859. Goette A. Über die Entwicklung der Hydromedusen. Zool Anz. 1904;27:473–5. Goette A. Vergleichende Entwicklungsgeschichte der Geschlechtsindividuen der Hydropolypen. Leipzig: Verlag von Wilhelm Engelmann; 1907. Allman GJ. A monograph of the gymnoblastic or tubularian hydroids: in two parts. The Hydroida in general. London: Ray Society. 1871;1:40–3. Metschnikoff E. Embryologische Studien an Medusen: Ein Beitrag zur Genealogie der Primitiv-organe. Wien: A. Hölder; 1886. Hadzi J. Bemerkungen zur Onto- und Phylogenie der Hydromedusen. Leipzig: Zool Anz. 1910;35:20–30. Siewing R, Wurmbach H. Lehrbuch der Zoologie: Jena VEB Gustav Fischer Verlag. 1985. Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, et al. Independent evolution of striated muscles in cnidarians and bilaterians. Nature. 2012;487(7406):231–4. Schulz MH, Zerbino DR, Vingron M, Birney E. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics. 2012;28(8):1086–92. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol. 2013;29(7):644. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, et al. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics. 2003;19(5):651–2. Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst E-M, et al. Regulation of polyp-to-jellyfish transition in Aurelia aurita. Curr Biol. 2014;24(3):263–73. Genikhovich G, Technau U. In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps. Cold Spring Harb Protoc. 2009;2009(9):pdb prot5282. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–8. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27(8):1164–5. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. Frey J. Die Entwicklungsleistungen der Medusenknospen und Medusen von Podocoryne carnea M Sars nach Isolation und Dissoziation. Wilhelm Roux’ Archiv. 1968;160(4):428–64. Tardent P. Coelenterata, Cnidaria. In: Seidel F, editor. Morphogenese der Tiere. Jena: VEB Gustav Fischer Verlag; 1978. Straehler-Pohl I. Die Phylogenie der Rhopaliophora (Scyphozoa und Cubozoa) und die Paraphylie der Rhizostomeae. Doctoral Thesis University of Hamburg: Faculty of Mathematics, Informatics and Natural Science; 2009. Kaestner A, Wetzel A, Gruner H-E. Lehrbuch der speziellen Zoologie. Jena: VEB Gustav Fischer Verlag; 1963. Scholz CB, Technau U. The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol. 2003;212(12):563–70. Fritzenwanker JH, Saina M, Technau U. Analysis of forkhead and snail expression reveals epithelial-mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol. 2004;275(2):389–402. Mazza ME, Pang K, Reitzel AM, Martindale MQ, Finnerty JR. A conserved cluster of three PRD-class homeobox genes (homeobrain, rx and orthopedia) in the Cnidaria and Protostomia. EvoDevo. 2010;1(1):3. Di Bernardo M, Castagnetti S, Bellomonte D, Oliveri P, Melfi R, Palla F, et al. Spatially restricted expression of PlOtp, a Paracentrotus lividus orthopedia-related homeobox gene, is correlated with oral ectodermal patterning and skeletal morphogenesis in late-cleavage sea urchin embryos. Development. 1999;126(10):2171–9. Arendt D, Technau U, Wittbrodt J. Evolution of the bilaterian larval foregut. Nature. 2001;409:81–5. Technau U. Brachyury, the blastopore and the evolution of the mesoderm. BioEssays. 2001;23(9):788–94. Tessmar-Raible K. The evolution of neurosecretory centers in bilaterian forebrains: insights from protostomes. Semin Cell Dev Biol. 2007;18:492–501. Stierwald M, Yanze N, Bamert RP, Kammermeier L, Schmid V. The Sine oculis/Six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration. Dev Biol. 2004;274(1):70–81. Spring J, Yanze N, Middel AM, Stierwald M, Gröger H, Schmid V. The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol. 2000;228(2):363–75. Reber-Muller S, Streitwolf-Engel R, Yanze N, Schmid V, Stierwald M, Erb M, et al. BMP2/4 and BMP5-8 in jellyfish development and transdifferentiation. Int J Dev Biol. 2006;50(4):377. Nakamura Y, Tsiairis CD, Özbek S, Holstein TW. Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer. Proc Natl Acad Sci. 2011;108(22):9137–42. Nakanishi N, Yuan D, Hartenstein V, Jacobs DK. Evolutionary origin of rhopalia: insights from cellular-level analyses of Otx and POU expression patterns in the developing rhopalial nervous system. Evol Dev. 2010;12(4):404–15. Spring J, Yanze N, Josch C, Middel AM, Winninger B, Schmid V. Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. Dev Biol. 2002;244(2):372–84. Smith KM, Gee L, Blitz IL, Bode HR. CnOtx, a member of the Otx gene family, has a role in cell movement in Hydra. Dev Biol. 1999;212(2):392–404. Technau U, Bode HR. HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development. 1999;126(5):999–1010. Reinhardt B, Broun M, Blitz IL, Bode HR. HyBMP5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra. Dev Biol. 2004;267(1):43–59. Martinez DE, Dirksen M-L, Bode PM, Jamrich M, Steele RE, Bode HR. Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in Hydra. Dev Biol. 1997;192(2):523–36. Mazza ME, Pang K, Martindale MQ, Finnerty JR. Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis. J Exp Zoolog B Mol Dev Evol. 2007;308(4):494–506. Collins AG. Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J Evol Biol. 2002;15:418–32. Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol. 2006;55(1):97–115.