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Morphological and molecular development of the eyes during embryogenesis of the freshwater planarian Schmidtea polychroa

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Abstract

Photoreception is one of the most primitive sensory functions in metazoans. Despite the diversity of forms and components of metazoan eyes, many studies have demonstrated the existence of a common cellular and molecular basis for their development. Genes like pax6, sine oculis, eyes absent, dachshund, otx, Rx and atonal are known to be associated with the specification and development of the eyes. In planarians, sine oculis, eyes absent and otxA play an essential role during the formation of the eye after decapitation, whereas pax6, considered by many authors as a master control gene for eye formation, does not seem to be involved in adult eye regeneration. Whether this is a peculiarity of adult planarians or, on the contrary, is also found in embryogenesis remains unknown. Herein, we characterize embryonic eye development in the planarian species Schmidtea polychroa using histological sections and molecular markers. Additionally, we analyse the expression pattern of the pax6–sine oculis–eyes absent–dachshund network, and the genes Rx, otxA, otxB and atonal. We demonstrate that eye formation in planarian embryos shows great similarities to adult eye regeneration, both at the cellular and molecular level. We thus conclude that planarian eyes exhibit divergent molecular patterning mechanisms compared to the prototypic ancestral metazoan eye.

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References

  • Abascal F, Zardoya R, Posada D (2005) Prottest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Agata K, Soejima Y, Kato K, Kobayashi C, Umesono Y, Watanabe K (1998) Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool Sci 15:433–440

    Article  PubMed  CAS  Google Scholar 

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Almuedo-Castillo M, Saló E, Adell T (2011) Dishevelled is essential for neural connectivity and planar cell polarity in planarians. Proc Nat Acad Sci U S A 108:2813–2818

    Article  CAS  Google Scholar 

  • Arenas-Mena C, Wong K (2007) HeOtx expression in an indirectly developing polychaete correlates with gastrulation by invagination. Dev Genes Evol 217:373–384

    Article  PubMed  CAS  Google Scholar 

  • Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563–571

    PubMed  Google Scholar 

  • Arendt D, Wittbrodt J (2001) Reconstructing the eyes of urbilateria. Phil Trans R Soc B 356:1545–1563

    Article  PubMed  CAS  Google Scholar 

  • 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 129:1143–1154

    PubMed  CAS  Google Scholar 

  • Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J (2004) Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306:869–871

    Article  PubMed  CAS  Google Scholar 

  • Callaerts P, Muñoz-Mármol AM, Glardon S, Castillo E, Sun H, Li WH, Gehring WJ, Saló E (1999) Isolation and expression of a Pax-6 gene in the regenerating and intact planarian Dugesia (G) tigrina. Proc Natl Acad Sci USA 96:558–563

    Article  PubMed  CAS  Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2005) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131

    Article  PubMed  Google Scholar 

  • Carpenter KS, Morita M, Best JB (1974) Ultrastructure of the photoreceptor of the planarian Dugesia dorotocephala. I. Normal eye. Cell Tissue Res 148:143–158

    Article  PubMed  CAS  Google Scholar 

  • Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A (1999) Pax6 induces ectopic eyes in a vertebrate. Development 126:4213–4222

    PubMed  CAS  Google Scholar 

  • Erclik T, Hartenstein V, McInnes RR, Lipshitz HD (2009) Eye evolution at high resolution: the neuron as a unit of homology. Dev Biol 332:70–79

    Article  PubMed  CAS  Google Scholar 

  • Frohman MA (1994) On beyond classic race (rapid amplification of cDNA ends). PCR Meth Appl 4:40–58

    Google Scholar 

  • Gehring WJ, Ikeo K (1999) Pax6: mastering eye morphogenesis and eye evolution. Trends Genet 15:371–377

    Article  PubMed  CAS  Google Scholar 

  • Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643

    Article  PubMed  CAS  Google Scholar 

  • Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792

    Article  PubMed  CAS  Google Scholar 

  • Hill RE, Favor J, Hogan BLM, Ton CCT, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354:522–525

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) Mrbayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hyman LH (1951) The invertebrates, vol II. Platyhelminthes and Rhynchocoela. McGraw-Hill, New York, chap The Platyhelminthes

    Google Scholar 

  • Iglesias M, Almuedo-Castillo M, Aboobaker A, Saló E (2011) Early planarian brain regeneration is independent of blastema polarity mediated by the Wnt/β-catenin pathway. Dev Biol 358:68–78

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of pax genes in eye evolution: a cnidarian paxb gene uniting pax2 and pax6 functions. Dev Cell 5:773–785

    Article  PubMed  CAS  Google Scholar 

  • Lapan SW, Reddien PW (2011) dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet 7:e1002–e1226

    Article  Google Scholar 

  • Le Moigne A (1963) Etude du développement embryonnaire de Polycelis nigra (Turbellarié, Triclade). Bull Soc Zool Fr 88:403–422

    Google Scholar 

  • Leys SP, Degnan BM (2001) Cytological basis of photosensitive behaviour in a sponge larva. Biol Bull 201:323–338

    Article  PubMed  CAS  Google Scholar 

  • Loosli F, Kmita-Cunisse M, Gehring WJ (1996) Isolation of a Pax-6 homolog from the ribbonworm Lineus sanguineus. Proc Natl Acad Sci U S A 93:2658–2663

    Article  PubMed  CAS  Google Scholar 

  • Mannini L, Rossi L, Deri P, Gremigni V, Salvetti A, Saló E, Batistoni R (2004) Djeyes absent (Djeya) controls prototypic planarian eye regeneration by cooperating with the transcription factor Djsix-1. Dev Biol 269:346–359

    Article  PubMed  CAS  Google Scholar 

  • Mannini L, Deri P, Picchi J, Batistoni R (2008) Expression of a retinal homeobox (Rx) gene during planarian regeneration. Int J Dev Biol 52:1113–1117

    Article  PubMed  CAS  Google Scholar 

  • Martín-Durán JM, Romero R (2011) Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol 352:164–176

    Article  PubMed  Google Scholar 

  • Martín-Durán JM, Duocastella M, Serra P, Romero R (2008) New method to deliver exogenous material into developing planarian embryos. J Exp Zool (Mol Dev Evol) 310B:668–681

    Article  Google Scholar 

  • Martín-Durán JM, Amaya E, Romero R (2010) Germ layer specification and axial patterning in the embryonic development of the freshwater planarian Schmidtea polychroa. Dev Biol 340:145–158

    Article  PubMed  Google Scholar 

  • Nishimura K, Kitamura Y, Inoue T, Umesono Y, Yoshimoto K, Takeuchi K, Taniguchi T, Agata K (2007) Identification and distribution of tryptophan hydroxylase (tph)-positive neurons in the planarian Dugesia japonica. Nuerosci Res 59:101–106

    Article  CAS  Google Scholar 

  • Passamaneck YJ, Furchheim N, Hejnol A, Martindale MQ, Luter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo 2:6

    Article  PubMed  CAS  Google Scholar 

  • Pineda D, González J, Callaerts P, Ikeo K, Gehring WJ, Saló E (2000) Searching for the prototypic eye genetic network: sine oculis is essential for eye regeneration in planarians. Proc Natl Acad Sci U S A 97:4525–4529

    Article  PubMed  CAS  Google Scholar 

  • Pineda D, González J, Marsal M, Saló E (2001) Evolutionary conservation of the initial eye genetic pathway in planarians. Belg J Zool 131(Supplement 1):77–82

    Google Scholar 

  • Pineda D, Rossi L, Batistoni R, Salvetti A, Marsal M, Gremigni V, Falleni A, González-Linares J, Deri P, Saló E (2002) The genetic network of prototypic planarian eye regeneration is pax6 independent. Development 129:1423–1434

    PubMed  CAS  Google Scholar 

  • Quigley IK, Xie X, Shankland M (2007) Hau-Pax6A expression in the central nervous system of the leech embryo. Dev Genes Evol 217:459–468

    Article  PubMed  CAS  Google Scholar 

  • Quigley IK, Schmerer MW, Shankland M (2010) A member of the six gene family promotes the specification of p cell fates in the o/p equivalence group of the leech Helobdella. Dev Biol 344:319–330

    Article  PubMed  CAS  Google Scholar 

  • Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265:785–789

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rossi L, Batistoni R, Salvetti A, Deri P, Bernini F, Andreoli I, Falleni A, Gremigni V (2001) Molecular aspects of cell proliferation and neurogenesis in planarians. Belg J Zool 131(Supplement 1):83–87

    Google Scholar 

  • Ruzickova J, Piatigorsky J, Kozmik Z (2009) Eye-specific expression of an ancestral jellyfish paxb gene interferes with pax6 function despite its conserved pax6/pax2 characteristics. Int J Dev Biol 53:469–482

    Article  PubMed  CAS  Google Scholar 

  • Sakai F, Agata K, Orii H, Watanabe K (2000) Organization and regeneration ability of spontaneous supernumerary eyes in planarians—eye regeneration field and pathway selection by optic nerves. Zool Sci 17:375–381

    PubMed  CAS  Google Scholar 

  • Salvini-Plawen L, Mayr E (1961) Evolutionary biology, vol 10. Plenum Press, New York, pp 207–263

    Google Scholar 

  • Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, Oxford, pp 118–147, chap Sensory organs

    Book  Google Scholar 

  • Sluys R (1989) A monograph of the marine triclads. Rotterdam & Brookfield, Rotterdam

    Google Scholar 

  • Steinmetz PRH, Kostyuchenko RP, Fischer A, Arendt D (2011) The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol Dev 13:72–79

    Article  PubMed  Google Scholar 

  • Stevens NM (1904) On the germ cells and the embryology of Planaria simplicissima. Proc Acad Nat Sci Philadelphia 56:208–220

    Google Scholar 

  • Takeda H, Nishimura K, Agata K (2009) Planarians maintain a constant ratio of different cell types during changes in body size by using the stem cell system. Zool Sci 26:805–813

    Article  PubMed  Google Scholar 

  • Tomarev SI, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring WJ, Piatigorsky J (1997) Squid Pax-6 and eye development. Proc Natl Acad Sci U S A 94:2421–2426

    Article  PubMed  CAS  Google Scholar 

  • 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 142:800–809

    Article  PubMed  CAS  Google Scholar 

  • Umesono Y, Watanabe K, Agata K (1997) A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain. Develop Growth Differ 39:723–727

    Article  CAS  Google Scholar 

  • Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209:31–39

    Article  PubMed  CAS  Google Scholar 

  • Vopalensky P, Kozmik Z (2009) Eye evolution: common use and independent recruitment of genetic components. Phil Trans R Soc B 364:2819–2832

    Article  PubMed  CAS  Google Scholar 

  • Winchell CJ, Valencia JE, Jacobs DK (2010) Expression of Distal-les, dachshund, and optomotor blind in Neanthes arenaceodentata (Annelida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria. Dev Genes Evol 220:275–295

    Article  PubMed  Google Scholar 

  • Yamamoto H, Agata K (2011) Optic chiasm formation in planarian I: cooperative netrin- and robo-mediated signals are required for the early stage of optic chiasm formation. Develop Growth Differ 53:300–311

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Vila-Farré and F. Cebrià for support and comments on this manuscript. JMM-D was an FPU fellow funded by the MICINN (Ministerio de Ciencia e Innovación), Spain. FM is an APIF fellow at the University of Barcelona, Spain. This work was supported by MEC BFU- 2007–63209, Spain, to RR.

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  1. José María Martín-Durán

    Present address: Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, 5008, Bergen, Norway

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  1. Departament de Genètica, Universitat de Barcelona, Avda. Diagonal 643, 08028, Barcelona, Spain

    José María Martín-Durán, Francisco Monjo & Rafael Romero

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  1. José María Martín-Durán
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  2. Francisco Monjo
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Correspondence to José María Martín-Durán.

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Communicated by D. Weisblat

José María Martín-Durán and Francisco Monjo contributed equally to this work.

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Martín-Durán, J.M., Monjo, F. & Romero, R. Morphological and molecular development of the eyes during embryogenesis of the freshwater planarian Schmidtea polychroa . Dev Genes Evol 222, 45–54 (2012). https://doi.org/10.1007/s00427-012-0389-5

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