Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 1, 2013, Pages 193-198

  Backfisch, Benjamin ^a   Rajan, Vinoth Babu Veedin ^a   Fischer, Ruth M ^a   Lohs, Claudia ^a,b   Arboleda, Enrique ^a,c   Tessmar Raible, Kristin ^a   Raible, Florian ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c Council on International Educational Exchange Research Station Bonaire ^*  (Netherlands)

Author keywords

Polychaete; Regulation; Transposon; Worm

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; OPSIN; PIGMENT; PLASMID DNA; PROTEIN OPN2M 2; PROTEIN OPN4X 2; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG;

ANIMAL; ANNELID; ARTICLE; BRAIN; CELL DIFFERENTIATION; DEVELOPMENTAL STAGE; EVOLUTION; GENE LOCUS; MECHANORECEPTOR; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PHOTORECEPTOR; PHOTORECEPTOR CELL; PLATYNEREIS DUMERILI; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENICS; VENTRAL ROOT; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BIOLOGICAL EVOLUTION; DNA PRIMERS; GENE EXPRESSION PROFILING; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; OPSINS; PHOTORECEPTOR CELLS, INVERTEBRATE; POLYCHAETA; SEQUENCE ANALYSIS, DNA; ZEBRAFISH;

ANIMALIA; ANNELIDA; BRANCHIOSTOMA LANCEOLATUM; DANIO RERIO; LOPHOTROCHOZOA; METAZOA; PLATYNEREIS; PLATYNEREIS DUMERILII; POLYCHAETA;

EID: 84871945626     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1209657109     Document Type: Article

References (53)

1. Salvini-Plawen L, Mayr E (1977) On the evolution of photoreceptors and eyes. Evol Biol 10:207-263.
2. Dzik J (2003) Early Cambrian lobopodian sclerites and associated fossils from Kazakhstan. Palaeontology 46(1):93-112.
3. Purschke G, Ding Z, Müller MC (1995) Ultrastructural differences as a taxonomic marker: The segmental ocelli of Polyophthalmus pictus and Polyophthalmus qingdaoensis sp.n. (Polychaeta, Opheliidae). Zoomorphology 115(4):229-241. (Pubitemid 126011535)
4. Hesse R (1899) Untersuchungen über die Organe der Lichtempfindung bei niederen Thieren. V. Die Augen der polychäten Anneliden [Studies on the light sensation in lower animals. V. The eyes of polychaete annelids]. Z Wiss Zool 65:446-516, German.
5. Xiang Y, et al. (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468(7326):921-926.
6. Ullrich-Lüter EM, Dupont S, Arboleda E, Hausen H, Arnone MI (2011) Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci USA 108(20):8367-8372.
7. Hesse R (1898) Untersuchungen über die Organe der Lichtempfindung bei niederen Thieren. IV. Die Sehorgane des Amphioxus [Studies on the light sensation in lower animals. IV. The visual organs of amphioxus]. Z Wiss Zool 65:456-464. German.
8. Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267(5205):1788-1792.
9. Gehring WJ (2011) Chance and necessity in eye evolution. Genome Biol Evol 3:1053-1066.
10. Purschke G, Arendt D, Hausen H, Müller MC (2006) Photoreceptor cells and eyes in Annelida. Arthropod Struct Dev 35(4):211-230. (Pubitemid 44883362)
11. Arendt D, Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond B Biol Sci 356(1414):1545-1563. (Pubitemid 33001680)
12. Raible F, et al. (2006) Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Dev Biol 300(1):461-475. (Pubitemid 44834389)
13. Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A (2005) Cephalochordate melanopsin: Evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol 15(11):1065-1069. (Pubitemid 40772156)
14. Vopalensky P, et al. (2012) Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye. Proc Natl Acad Sci USA 109(38):15383-15388.
15. Kozmik Z (2005) Pax genes in eye development and evolution. Curr Opin Genet Dev 15(4):430-438.
16. Mishra M, et al. (2010) Pph13 and orthodenticle define a dual regulatory pathway for photoreceptor cell morphogenesis and function. Development 137(17):2895-2904.
17. Glardon S, Holland LZ, Gehring WJ, Holland ND (1998) Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): Insights into eye and photoreceptor evolution. Development 125(14):2701-2710. (Pubitemid 28396167)
18. Arendt D, Tessmar K, de Campos-Baptista MI, Dorresteijn A, Wittbrodt J (2002) Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129(5):1143-1154.
19. Tessmar-Raible K, et al. (2007) Conserved sensory-neurosecretory cell types in annelid and fish forebrain: Insights into hypothalamus evolution. Cell 129(7):1389-1400. (Pubitemid 46970710)
20. Denes AS, et al. (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129(2):277-288. (Pubitemid 46584732)
21. Jékely G, et al. (2008) Mechanism of phototaxis in marine zooplankton. Nature 456 (7220):395-399.
22. Tomer R (2008) The Evolution of Mushroom Body and Telencephalic Cell Types, Studied by Single Cell Expression Profiling of Platynereis dumerilii Larvae (University of Heidelberg, Heidelberg).
23. Medhora M, Maruyama K, Hartl DL (1991) Molecular and functional analysis of the mariner mutator element Mos1 in Drosophila. Genetics 128(2):311-318.
24. Raible F, et al. (2005) Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310(5752):1325-1326. (Pubitemid 41698863)
25. Rhode B (1992) Development and differentiation of the eye in Platynereis dumerilii (Annelida, Polychaeta). J Morphol 212:71-85.
26. Dorresteijn A (2005) Cell lineage and gene expression in the development of polychaetes. Hydrobiologia 535/536:1-22.
27. Hauenschild C, Fischer A (1969) Platynereis dumerilii. Mikroskopische Anatomie, Fortpflanzung und Entwicklung [Platynereis dumerilii. Microscopical anatomy, reproduction and development]. Grosses Zoologisches Praktikum, (G. Fischer Verlag, Stuttgart). German.
28. Bullock TH, Horridge GA (1965) Stucture and Function in the Nervous Systems of Invertebrates (Freeman, San Francisco), p 1719.
29. Hofmann DK (1976) Regeneration and endocrinology in the polychaete Platynereis dumerilii. An experimental and structural study. Roux Arch Dev Biol 180(1):47-71.
30. Tessmar-Raible K, Steinmetz PR, Snyman H, Hassel M, Arendt D (2005) Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development. Biotechniques 39(4):460-464, 462, 464.
31. Saudemont A, et al. (2008) Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis. Dev Biol 317(2):430-443.
32. Tomer R, Denes AS, Tessmar-Raible K, Arendt D (2010) Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142(5):800-809.
33. Winchell CJ, Valencia JE, Jacobs DK (2010) Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata (Annelida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria. Dev Genes Evol 220(9-10):275-295.
34. Arendt D (2008) The evolution of cell types in animals: Emerging principles from molecular studies. Nat Rev Genet 9(11):868-882.
35. Xiao T, Roeser T, Staub W, Baier H (2005) A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132(13):2955-2967. (Pubitemid 41086731)
36. Davies WI, et al. (2011) Functional diversity of melanopsins and their global expression in the teleost retina. Cell Mol Life Sci 68(24):4115-4132.
37. Hermans CO (1969) Fine structure of the segmental ocelli of Armandia brevis (Polychaeta: Opheliidae). Z Zellforsch Mikrosk Anat 96(3):361-371.
38. Kozmik Z, et al. (2007) Pax-Six-Eya-Dach network during amphioxus development: Conservation in vitro but context specificity in vivo. Dev Biol 306(1):143-159. (Pubitemid 46809720)
39. Candiani S, et al. (2003) Cloning and developmental expression of amphioxus Dachschund. Gene Expr Patterns 3(1):65-69. (Pubitemid 36356044)
40. Kawakami K, Sato S, Ozaki H, Ikeda K (2000) Six family genes - structure and function as transcription factors and their roles in development. Bioessays 22(7):616-626. (Pubitemid 30457953)
41. Zuber ME, Gestri G, Viczian AS, Barsacchi G, Harris WA (2003) Specification of the vertebrate eye by a network of eye field transcription factors. Development 130(21):5155-5167. (Pubitemid 37369675)
42. Nilsson DE (2004) Eye evolution: A question of genetic promiscuity. Curr Opin Neurobiol 14(4):407-414. (Pubitemid 39078486)
43. Remane A (1955) Morphologie als Homologienforschung [Morphology as homology research]. Zool Anz (Suppl. 18):159-183. German.
44. Blackburn DC, et al. (2008) Isolation and expression of Pax6 and atonal homologues in the American horseshoe crab, Limulus polyphemus. Dev Dyn 237(8):2209-2219.
45. Pineda D, et al. (2002) The genetic network of prototypic planarian eye regeneration is Pax6 independent. Development 129(6):1423-1434. (Pubitemid 34874163)
46. Schlosser G (2010) Making senses development of vertebrate cranial placodes. Int Rev Cell Mol Biol 283:129-234.
47. Senthilan PR, et al. (2012) Drosophila auditory organ genes and genetic hearing defects. Cell 150(5):1042-1054.
48. Fu W, Duan H, Frei E, Noll M (1998) shaven and sparkling are mutations in separate enhancers of the Drosophila Pax2 homolog. Development 125(15):2943-2950. (Pubitemid 28410218)
49. Fritzsch B, et al. (2005) Ancestry of photic and mechanic sensation? Science 308(5725):1113-1114.
50. Niwa N, Hiromi Y, Okabe M (2004) A conserved developmental program for sensory organ formation in Drosophila melanogaster. Nat Genet 36(3):293-297. (Pubitemid 38282756)
51. Montell C (2012) Drosophila visual transduction. Trends Neurosci 35(6):356-363.
52. Fischer A (1965) Über die Chromatophoren und den Farbwechsel bei dem Polychäten Platynereis dumerilii [About the chromatophores and the color change in the polychaete Platynereis dumerilii]. Z Zellforsch Mikrosk Anat 65:290-312. German.
53. Tessmar-Raible K, Raible F, Arboleda E (2011) Another place, another timer: Marine species and the rhythms of life. Bioessays 33(3):165-172.