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WIREs Dev Biol
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The evolution of vision

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In this review, the evolution of vision is retraced from its putative origins in cyanobacteria to humans. Circadian oscillatory clocks, phototropism, and phototaxis require the capability to detect light. Photosensory proteins allow us to reconstruct molecular phylogenetic trees. The evolution of animal eyes leading from an ancestral prototype to highly complex image forming eyes can be deciphered on the basis of evolutionary developmental genetic experiments and comparative genomics. As all bilaterian animals share the same master control gene, Pax6, and the same retinal and pigment cell determination genes, we conclude that the different eye‐types originated monophyletically and subsequently diversified by divergent, parallel, or convergent evolution. WIREs Dev Biol 2014, 3:1–40. doi: 10.1002/wdev.96

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Figure 1.

The molecular circadian clock of Drosophila. Upper panel: Abundance profiles of head mRNA (dashed lines) and protein (solid lines) for rhythmic components of the core oscillator mechanism. Numbers indicate Zeitgeber time (ZT), where 0–12 = lights on (white bar) and 12–24/0 = lights off (black bar). mRNA transcripts that peak in the morning (blue) and evening (orange) are shown with the main cis‐regulatory DNA sequence that is targeted to generate rhythmic expression indicated above each peak. CRY protein is not shown, although it is degraded by light and, therefore, accumulates during the night. The CYC protein levels are constitutive due to constant cyc expression. Lower panel: Flow diagram showing transcriptional regulation from left to right and feedback from right to left in the core circadian mechanism. The panels are aligned and color coded so that the interactions can be correlated with the abundance profiles, which they generate. Key: solid arrows = up‐regulation; blunt‐ended lines = down‐regulation; dashed arrows = transcription/translation; dotted line = probable interaction between CRY and PER in the dark; lightning bolt depicts light‐induced activation of CRY; inset depicts the major transcription factor families which are involved. (Reprinted with permission from Ref 29. Copyright 2011 the Biochemical Society)

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Figure 2.

The eyespot of Chlamydomonas. (a) A Chlamydomonas cell with two flagella, a large green chloroplast and a yellow‐orange eyespot (eye organelle). (b) Function of the eyespot, Channelrhodopsin 1 (ChR1) is a light‐gated proton channel located in the plasma membrane above the pigment spot. The entering protons diffuse laterally and activate a voltage or proton‐gated Ca++ channel (NGCC). Channelrhodopsin 2 (ChR2) is conductive for H+, Na+ and Ca++. The voltage change ΔΨ is transmitted along the membrane and sensed by the VGCC channels in the flagellar membrane. A sudden Ca influx induces a switch of flagellar motion. The carotene reflects the light to activate the ChRs. (Reprinted with permission from Ref 54. Copyright 2004 American Physiological Society)

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Figure 3.

Phylogenetic tree of the family of cryptochromes/photolyases. Upper panel: Domain structure of cryptochromes and photolyases from Escherichia coli and Arabidopsis thaliana (At), respectively. The N‐terminal domain which binds two chromophores methenyltetrahydrofolate (MTHF) and flavin adenine dinucleotide (FAD) shown in yellow is highly conserved among all classes of cryptochromes and photolyases. By contrast, the c‐terminal extension (black) is variable and not found in photolyases. Lower panel: Phylogenetic tree of cryptochromes/photolyases. Green: plant cryptochromes. Pink and violet: two groups of animal cryptochromes. Blue: DASH cryptochromes and some related proteins. Red, brown, and gray: CPD photolyases classes I, II, and III. An asterisk (*) marks dual‐type belonging to either class I CPD or (6‐4) photolyases capable of DNA repair, but they also possess photoreceptor activity. CPD, cyclobutane pyrimidine dimer; DASH, Drosophila, Arabidopsis, Synechocystis, Homo. (Reprinted with permission from Ref . Copyright 2011 Annual Reviews Inc)

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Figure 4.

Unrooted phylogenetic tree of microbial rhodopsins. Source: Hiroshi Suga.

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Figure 5.

Structure and function of various microbial rhodopsins. Proteorhodopsin, halorhodopsin, sensory rhodopsin of Anabaena and the two channelopsins function as ion channels, whereas sensory rhodopsin I is coupled to a transducer complex, which transmits the light signal via a histidine kinase and phosphorylates a regulator of the flagellar motor. (Reprinted with permission from Ref 105. Copyright 2005 Wiley‐VCH)

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Figure 6.

Schematic representation of bovine rhodopsin inserted in the disc membrane. On the basis of crystallographic data. H1–H7, transmembrane α‐helices; H8, short cytoplasmic α‐helix. (Reprinted with permission from Ref 127. Copyright 2005 Wiley‐VCH)

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Figure 7.

Phylogenetic tree of animal opsins. Maximum likelihood tree. Shaded areas represent cnidarian rhodopsins. Source: Suga et al.

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Figure 8.

G‐protein coupled signal transduction in ciliary and rhabdomeric photoreceptors. (a) In ciliary photoreceptors, c‐opsin receives the light signal and transmits it via a trimeric G‐protein complex to phosphodiesterase (PDE) which leads to a decrease in cGMP levels and to a closure of cGMP‐gated channels in the plasma membrane. Ciliary photoreceptor form membrane stacks (discs) from the ciliary membrane. By contrast (b) rhabdomeric photoreceptors transmit the light signal from r‐opsins via a different G‐protein complex to phospholipase C (PLC) which cleaves phosphoinositol (PIP2) leading to an increase in intracellular calcium and the opening of Na+, Ca++ channels and depolarization of the plasma membrane. Rhabdomeric photoreceptor form membrane stacks from microvilli. (Reprinted with permission from Ref . Copyright 1997 Blackwell Science)

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Figure 9.

Eye organelles of the unicellular dinoflagellates Erythropsis and Warnovia. (a) Erythropsis, (b) eye organelle of Erythropsis, (c) Warnovia, (d) eye organelle of Warnovia, (e) nucleus and eye organelle of Warnovia, and (f) birefringence in the retina‐like structure detected by polarized light in Warnovia. (a–f) Source: Makiko Seimiya and Jean and Colette Febvre. (g) Ultrastructure of the eye organelle of Warnovia and (h) ultrastructure of the retina‐like structure with regularly stacked membranes and large pigment granules. (g and h: Reprinted with permission from Ref . Copyright 1969)

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Figure 10.

Unicellular photoreceptors in the planula larva of the box jellyfish Tripedalia. (a) Planula larva and (b) unicellular photoreceptor with pigment granules, microvilli, and a flagellum. (Reprinted with permission from Ref 81. Copyright 2003 Royal Society Publishing)

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Figure 11.

Protypic eyes (E) in (a) the planarian Polycelis auricularia, (b and c) higher magnification, (d) histological section across the eye of Planaria torva. Pc, pigment cell; PcN, pigment cell nucleus; Mv, microvilli; Ph, photoreceptor cell; PhN, photoreceptor cell nucleus. (Reprinted with permission from Ref . Copyright 1897 Royal Society of London)

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Figure 12.

General scheme of eye evolution. The first step in eye evolution is the evolution of a light receptor molecule which in all metazoa is rhodopsin. In the most ancestral metazoa, the sponges, a single Pax gene, but no opsin gene has been found. In the larva of the box jellyfish Tripedalia, a unicellular photoreceptor has been described. The adult jellyfish forms complex lens eye with ciliary photoreceptor cells, which form under control of PaxB, a putative precursor of Pax6. However, the eyes of the hydrozoan jellyfish Cladonema are controlled by PaxA. We propose that the prototypic eye consisting of just two cells a photoreceptor cell and a pigment cell originated from a unicellular photoreceptor by a first step of cell differentiation. This cellular differentiation led to formation of a photoreceptor cell and a pigment cell under the genetic control by Pax6 and Mitf, respectively. As true innovations are rare in evolution all the more complex eye‐types arose monophyletically from one of these Darwinian prototypes leading to a large diversity of eye‐types by divergence, parallel evolution, and convergence.

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Figure 13.

Induction of ectopic eyes in Drosophila by targeted expression of the Pax6 homologs eyeless (ey) and twin of eyeless (toy). (a) Experimental design: targeted expression of ey c‐DNA using a genomic enhancer to induce the yeast Gal4 transcription factor in various imaginal discs. Gal4 binds to the upstream activating sequences (UAS) and drives the expression of ey into the respective areas of the eye‐antennal, wing, and leg discs, respectively. (b) Ectopic eyes induced by ey. (c) Ectopic eyes induced by toy. Source: Urs Kloter and Georg Halder

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Figure 14.

Initiation of the developmental pathway for compound eye and ocelli development. Pax6 homologs toy and ey are on top of the hierarchy, so and eya as well as dac are second‐order transcription factors connected by various feedback loops to the master control genes ey and toy. In ocellar development, an additional master control gene otd is required. toy, twin of eyeless; ey, eyeless; eyg, eyegone; optix; so, sine oculis; eya, eyes absent; dac, dachshund; otd, othodenticle; hh, hedgehog.

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Figure 15.

Phylogenetic tree of the six/so gene family. The phylogenetic analysis shows that a given transcription factor can regulate any developmental program as long as the target genes possess the appropriate cis‐regulatory elements. The six1 and six3 subclasses (blue) both regulate eye development in Drosophila as well as in vertebrates, whereas the six4 subclass (red) controls muscle development. h, human; m, mouse; D, Drosophila, zf, zebrafish, c, ciona; mf, medaka; e, C. elegans.

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Figure 16.

Deciphering the eye developmental program by analyzing the transcriptome. Genes that are expressed specifically in eye discs as compared to leg disc are listed for the larval, pupal, and adult stages. At the larval stage particularly transcription factor genes are expressed which initiate the eye developmental pathway. At the pupal stage mostly structural genes are activated as well as genes involved in the synthesis of eye pigments. In the adult animal mainly genes involved in intracellular signaling, neurotransmission, and the visual process are expressed. In total, approximately 1000 genes are required for eye development and maintenance. Source: Michaut and Gehring, unpublished data.

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Figure 17.

Positioning of the eye in head region of the Drosophila embryo. Proposed model for the onset of toy expression. toy is activated (arrows) by the maternal effect genes bicoid (bcd) which forms a protein gradient and torso (tor). It is repressed from all sides by hunchback (hb), knirps (kni), and decapentaplegic (dpp). The posterior repressor remains to be identified.

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