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Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria

Detlev Arendt¹, Kristin Tessmar^1,*, Maria-Ines Medeiros de Campos-Baptista¹, Adriaan Dorresteijn² and Joachim Wittbrodt^1,

¹ European Molecular Biology Laboratory, Meyerhofstraße 1, 69117 Heidelberg, Germany
² Institut fuer Allgemeine und Spezielle Zoologie, Justus-Liebig-Universität, Stephanstr. 24, 35390 Giessen, Germany
^* Present address: Department of Biochemistry and Biophysics, University of California San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143, USA

View larger version (96K): [in a new window]   Fig. 1. Larval and adult eye development in Platynereis dumerilii. Ultrastructure of larval (A, 24 hours) and adult (B,C) eyes at 72 hours (B) and fully grown (C). Redrawn from EM micrographs (A,B; data not shown) and (C) after Fischer and Brökelmann (Fischer and Brökelmann, 1966). Yellow, rhabdomeric photoreceptor cells; green, pigment cells. (D) Photomicrograph of 24 hour trochophora showing the yellow natural pigment of larval eyes (white arrows). (E) Larval (white arrows) and adult eyes at 72 hours. Green autofluorescence marks pigment cells of adult eye (black arrow). (F-H) Staining of axonal scaffold with anti-acetylated tubulin antibody. Apical view showing larval axons and enervation of larval eyes at 36 hours of development (F). Axonal scaffold at 48 hours (G) and 72 hours (H), apical views. Black arrows, adult eyes. Abbreviations: aen, adult eye nerve; len, larval eye nerve; oc, optic commissure; plp, palpae anlagen; prn, prototroch ring nerve.

View larger version (75K): [in a new window]   Fig. 2. Pd-pax6, Pd-six1/2, Pd-ath and Pd-opsin alignments. Alignment of protostome and deuterostome pax6 (A), six1/2 (B), atonal (C) and opsin (D) protein sequences. Conserved domains are indicated by a bar. Identical amino acids are indicated by a dot in the alignments, gaps are represented by ‘-’. Abbreviations: I to VII, conserved transmembrane domains in r-opsin; bHLH, basic helix loop helix; HD, homeodomain; PD, paired domain; SD, six domain.

View larger version (35K): [in a new window]   Fig. 3. Phylogenetic trees. Trees were calculated using amino acid sequences. Numbers at branching points are bootstrap values exceeding 500. (A) Phylogenetic tree of Pax6 proteins. Platynereis Pax6 is closest to the other lochotrophozoan Pax6 proteins described so far. (B) Phylogenetic tree of Six/Sine oculis proteins. Platynereis six1/2 clearly clusters within the Six1/Six2 subfamily. (C) Phylogenetic analysis of Atonal-related proteins shows close relationship of Platynereis ath with Drosophila atonal. (D) Clear distinction between rhabdomeric (r-) and ciliary (c-) opsis revealed by phylogenetic analysis. Platynereis opsin is a member of the r-opsins subgroup.

View larger version (97K): [in a new window]   Fig. 4. Platynereis pax6, Pd-six1/2 and Pd-atonal in larval eye development. Apical views of whole-mount in situ stained embryos showing the pattern pax6 (A,D,G,K), six1/2 (B,E,H,L) and atonal (ath) (C,F,I,M) expression at 15 hours (A-C), 19 hours (D-F), 24 hours (G-I) and 36 hours of development (K-M). In 36-hour-old larvae (K-M), the axonal scaffold was counterstained with anti-acetylated tubulin antibody. Developing or mature larval eyes are indicated by white arrows. Black arrowheads point at isolated dorsal cells constantly expressing pax6.

View larger version (85K): [in a new window]   Fig. 5. Pd-six1/2, Pd-atonal and Pd-opsin at the onset of photoreceptor differentiation at 43 hours. Apical views at 43 hours of development. Expression of six1/2 (A) pax6 (B), ath (C) and r-opsin (D) in the differentiating adult eye. Black arrowheads point at isolated dorsal cells constantly expressing pax6. Cellular resolution of the whole-mount in situ analysis and the determinate development of Platynereis allow the direct comparison of the expression patterns using morphological landmarks (schematic drawings in the middle part of the figure).

View larger version (108K): [in a new window]   Fig. 6. Adult eye development in 2-day-old metatrochophora larvae. Apical views at 48 hours of development. Expression of pax6 (A) six1/2 (B) and r-opsin (C) in the growing adult eye. Black arrowheads indicate isolated dorsal cells constantly expressing pax6. (D) Schematic drawing of gene expression patterns at 48 hours of development. Natural pigment (brown spots) serves as morphological landmark. Abbreviations: ae, adult eyes; le, larval eyes; oa, optic anlagen; oc, optic commissure; ant, antennae; plp, palpae anlagen.

View larger version (56K): [in a new window]   Fig. 7. pax6 expression in the 72 hour episphere. Figure shows pax6 expression in 72 hour young worms in a series of optical sections from a ventroanterior view. (A) Surface view showing pax6 expression in larval eyes (white arrows), antennae (ant) and palpae (plp). (B) Deeper optical section with pax6 expression in larval eyes (le, white arrows) and anlagen of the palpae. (C) More dorsal optical section showing pax6 expression in antennae (ant), besides prominent expression in palpae.

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