Abstract
Unlike the compound eyes in insects, collembolan eyes are comparatively simple: some species have eyes with different numbers of ocelli (1 + 1 to 8 + 8), and some species have no apparent eye structures. Pax6 is a universal master control gene for eye morphogenesis. In this study, full-length Pax6 cDNAs, Fc-Pax6 and Cd-Pax6, were cloned from an eyeless collembolan (Folsomia candida, soil-dwelling) and an eyed one (Ceratophysella denticulata, surface-dwelling), respectively. Their phylogenetic positions are between the two Pax6 paralogs in insects, eyeless (ey) and twin of eyeless (toy), and their protein sequences are more similar to Ey than to Toy. Both Fc-Pax6 and Cd-Pax6 could induce ectopic eyes in Drosophila, while Fc-Pax6 exhibited much weaker transactivation ability than Cd-Pax6. The C-terminus of collembolan Pax6 is indispensable for its transactivation ability, and determines the differences of transactivation ability between Fc-Pax6 and Cd-Pax6. One of the possible reasons is that Fc-Pax6 accumulated more mutations at some key functional sites of C-terminus under a lower selection pressure on eye development due to the dark habitats of F. candida. The composite data provide a first molecular evidence for the monophyletic origin of collembolan eyes, and indicate the eye degeneration of collembolans is caused by adaptive evolution.
Highlights
Unlike the compound eyes in insects, collembolan eyes are comparatively simple: some species have eyes with different numbers of ocelli (1 + 1 to 8 + 8), and some species have no apparent eye structures
For collembolan Pax[6], we explored the induction assays with the constructs of gradual deletions from the C-termini of Fc-Pax[6] and Cd-Pax[6], respectively, to check the change of their transactivation ability
Some studies identified photosensitive organs that develop independently of Pax[6], e.g. larval eyes of Drosophila[39,40], the recent study of ey and toy knockdown in Tribolium embryo suggested both genes are required for the ocular segment, and the evolution of Pax6-independence of larval eye development in Drosophila involved further gene regulatory reorganization from the ancestral direct dependence on Pax[6] activity during specification[41]
Summary
Unlike the compound eyes in insects, collembolan eyes are comparatively simple: some species have eyes with different numbers of ocelli (1 + 1 to 8 + 8), and some species have no apparent eye structures. The discovery of Pax[6] as a universal master control gene for eye development throughout the animal kingdom supports the hypothesis of the monophyletic origin of different eye types[3,4]. Ectopic vertebrate eye structures can be induced by expressing the Drosophila ey or toy genes in Xenopus embryos[28] These studies suggest that the highly conserved Pax[6] controls the development of various types of eyes in both invertebrates and vertebrates. To date, functional studies of Pax[6] in relatively primitive hexapods are few, especially for comparative studies of closely-related species with distinct eye phenotypes
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