Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria.
The role of Pax6 in eye development in insects and vertebrates supports the view that their eyes evolved from simple pigment-cup ocelli present in their last common ancestors (Urbilateria). The cerebral eyes in errant polychaetes represent prototype invertebrate pigment-cup ocelli and thus resemble the presumed ancestral eyes. We have analysed expression of conserved eye specification genes in the early development of larval and adult pigment-cup eyes in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa). Both larval and adult eyes form in close vicinity of the optic anlagen on both sides of the developing brain ganglia. While pax6 is expressed in the larval, but not in the developing, adult eyes, expression of six1/2 from trochophora stages onwards specifically outlines the optic anlagen and thus covers both the developing larval and adult eyes. Using Platynereis rhabdomeric opsin as differentiation marker, we show that the first pair of adult eye photoreceptor cells is detected within bilateral clusters that transitorily express ath, the Platynereis atonal orthologue, thus resembling proneural sensory clusters. Our data indicate that--similar to insects, but different from the vertebrates--polychaete six1/2 expression outlines the entire visual system from early developmental stages onwards and ath-positive clusters generate the first photoreceptor cells to appear. We propose that pax6-, six1/2- and ath-positive larval eyes, as found in today's trochophora, were present already in Urbilateria.
Arendt
Detlev
D
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
Tessmar
Kristin
K
de Campos-Baptista
Maria-Ines Medeiros
MI
Dorresteijn
Adriaan
A
Wittbrodt
Joachim
J
D000595:Amino Acid Sequence; D000818:Animals; D051792:Basic Helix-Loop-Helix Proteins; D005075:Biological Evolution; D002628:Chemoreceptor Cells / Q000254:growth & development; D004268:DNA-Binding Proteins / Q000235:genetics; D005123:Eye / Q000254:growth & development*; D005136:Eye Proteins; D018398:Homeodomain Proteins / Q000235:genetics; D007814:Larva; D008969:Molecular Sequence Data; D009419:Nerve Tissue Proteins / Q000235:genetics; D000071841:PAX6 Transcription Factor; D051761:Paired Box Transcription Factors; D017956:Photoreceptor Cells, Invertebrate / Q000254:growth & development*; D011077:Polychaeta / Q000254:growth & development*; D012097:Repressor Proteins; D017299:Rod Opsins / Q000235:genetics; D017386:Sequence Homology, Amino Acid
D051792:Basic Helix-Loop-Helix Proteins; D004268:DNA-Binding Proteins; D005136:Eye Proteins; D018398:Homeodomain Proteins; D009419:Nerve Tissue Proteins; D000071841:PAX6 Transcription Factor; D051761:Paired Box Transcription Factors; D012097:Repressor Proteins; D017299:Rod Opsins; C500942:ATOH1 protein, human; C000605730:PAX6 protein, human; C484762:SIX2 protein, human