Abstract
BackgroundTranscription factors that determine retinal development seem to be conserved in different phyla throughout the animal kingdom. In most representatives, however, only a few of the involved transcription factors have been sampled and many animal groups remain understudied. In order to fill in the gaps for the chelicerate group of arthropods, we tested the expression pattern of the candidate genes involved in the eye development in the embryo of the wandering spider Cupiennius salei. One main objective was to profile the molecular development of the eyes and to search for possible variation among eye subtype differentiation. A second aim was to form a basis for comparative studies in order to elucidate evolutionary pathways in eye development.ResultsWe screened the spider embryonic transcriptome for retina determination gene candidates and discovered that all except one of the retinal determination genes have been duplicated. Gene expression analysis shows that the two orthologs of all the genes have different expression patterns. The genes are mainly expressed in the developing optic neuropiles of the eyes (lateral furrow, mushroom body, arcuate body) in earlier stages of development (160 to 220 h after egg laying). Later in development (180 to 280 h after egg laying), there is differential expression of the genes in disparate eye vesicles; for example, Cs-otxa is expressed only in posterior-lateral eye vesicles, Cs-otxb, Cs-six1a, and Cs-six3b in all three secondary eye vesicles, Cs-pax6a only in principal eye vesicles, Cs-six1b in posterior-median, and posterior-lateral eye vesicles, and Cs-six3a in lateral and principal eye vesicles.ConclusionsPrinciple eye development shows pax6a (ey) expression, suggesting pax6 dependence, although secondary eyes develop independently of pax6 genes and show differential expression of several retinal determination genes. Comparing this with the other arthropods suggests that pax6-dependent median eye development is a ground pattern of eye development in this group and that the ocelli of insects, the median eyes of chelicerates, and nauplius eyes can be homologised. The expression pattern of the investigated genes makes it possible to distinguish between secondary eyes and principal eyes. Differences of gene expression among the different lateral eyes indicate disparate function combined with genetic drift.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0010-x) contains supplementary material, which is available to authorized users.
Highlights
Transcription factors that determine retinal development seem to be conserved in different phyla throughout the animal kingdom
The eye vesicles of the secondary eyes (SEs) already form on the prosomal shield before it has reached the position of the optic neuropils, and the eye vesicles migrate with the prosomal shield, eventually ending up on top of the optic neuropil anlagen (Figure 2F,G)
The two pax6 genes show homology to ey and toy and demonstrate divergent expression patterns. This differential expression pattern is true for the remaining duplicated genes, namely six1, six3, atn, otx, and dac
Summary
Transcription factors that determine retinal development seem to be conserved in different phyla throughout the animal kingdom. The earliest target genes of ey have been categorized as ‘early retinal genes’ because their temporal expression extends from stages including the undifferentiated eye primordium to the differentiating retina [4] This group of RDGN genes includes the six1/2 homeobox gene sine oculis (so), optix orthologs or six homeobox genes, the nuclear haloacid dehalogenase group phosphatase eyes absent (eya), and the Ski/Snorelated transcriptional co-factor dachshund (dac) [16]. Formation of ocelli requires atn function [19] Another crucial gene with an conserved role in eye and photoreceptor cell development is the orthodenticle/otx gene. Otx orthologs are required for the formation of many retinal cell types [20] They are expressed in the photoreceptors of the fly ommatidia, ocelli, and Bolwig organ [21]. It is involved in polychaete eye formation [9] but shows no expression in either the developing planarian [29] or the onychophoran eyes [11]
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