Opsins in<i>Limulus</i>eyes: Characterization of three visible light-sensitive opsins unique to and co-expressed in median eye photoreceptors and a peropsin/RGR that is expressed in all eyes

Battelle, Barbara‐Anne; Kempler, K; Saraf, Spencer R.; Marten, Catherine E.; Dugger, Donald; Speiser, Daniel I.; Oakley, Todd H.

doi:10.1242/jeb.116087

Cited by 13 publications

(24 citation statements)

References 81 publications

(123 reference statements)

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“…Peropsins are expressed in the retina of several vertebrates [ 71 , 72 ] and amphioxus [ 73 ] where it is proposed to function as a retinal photoisomerase. Clear protostome peropsin orthologues have only been identified in spiders [ 74 , 75 ] and in the American horseshoe crab L. polyphemus [ 76 ]. We detect Pt-peropsin expression in the embryonic anlagen of lateral and median eyes, suggesting an early involvement in visual system development or function.…”

Section: Discussionmentioning

confidence: 99%

Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum

Schomburg

Turetzek

Schacht

et al. 2015

EvoDevo

108

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BackgroundTwo visual systems are present in most arthropod groups: median and lateral eyes. Most of our current knowledge about the developmental and molecular mechanisms involved in eye formation in arthropods comes from research in the model system Drosophila melanogaster. Here, a core set of retinal determination genes, namely, sine-oculis (so), eyes absent (eya), dachshund (dac), and the two pax6 orthologues eyeless (ey) and twin of eyeless (toy) govern early retinal development. By contrast, not much is known about the development of the up-to-eight eyes present in spiders. Therefore, we analyzed the embryonic expression of core retinal determination genes in the common house spider Parasteatoda tepidariorum.ResultsWe show that the anlagen of the median and lateral eyes in P. tepidariorum originate from different regions of the non-neurogenic ectoderm in the embryonic head. The median eyes are specified as two individual anlagen in an anterior median position in the developing head and subsequently move to their final position following extensive morphogenetic movements of the non-neurogenic ectoderm. The lateral eyes develop from a more lateral position. Intriguingly, they are specified as a unique field of cells that splits into the three individual lateral eyes during late embryonic development. Using gene expression analyses, we identified a unique combination of determination gene expression in the anlagen of the lateral and median eyes, respectively.ConclusionsThis study of retinal determination genes in the common house spider P. tepidariorum represents the first comprehensive analysis of the well-known retinal determination genes in arthropods outside insects. The development of the individual lateral eyes via the subdivision of one single eye primordium might be the vestige of a larger composite eye anlage, and thus supports the notion that the composite eye is the plesiomorphic state of the lateral eyes in arthropods. The molecular distinction of the two visual systems is similar to the one described for compound eyes and ocelli in Drosophila, suggesting that a unique core determination network for median and lateral eyes, respectively, might have been in place already in the last common ancestor of spiders and insects.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0011-9) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum

Schomburg

Turetzek

Schacht

et al. 2015

EvoDevo

108

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“…The "DRY" and "NPXXY" motifs, which are highly conserved among G-protein coupled receptors, are indicated by symbols + and $, respectively. crab Limulus polyphemus; Nagata et al, 2010;Eriksson et al, 2013;Battelle et al, 2015) and Crustacea (the Branchiura A. siamensis and the Copedoda Calanus finmarchicus; Sahoo et al, 2013;Lenz et al, 2014) species. Interestingly, EsPeropsin is expressed both in eye and in abdomen.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, we have identified a Peropsin homologue. Peropsin is a non-visual opsin member of Group 4 opsins previously described in vertebrates, Cephalochordata and Artropoda and a retinal-photoisomerase activity has been proposed as its main function (Sun et al, 1997;Koyanagi et al, 2002;Nagata et al, 2010;Eriksson et al, 2013;Battelle et al, 2015, Lenz et al, 2014Henze and Oakley, 2015). Furthermore, using qPCR on RNA isolated from compound eyes, brain and abdomen we detected the tissue expression of the newly identified opsins.…”

Section: Introductionmentioning

confidence: 98%

The opsin repertoire of the Antarctic krill Euphausia superba

et al. 2016

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The Antarctic krill Euphausia superba experiences almost all marine photic environments throughout its life cycle. Antarctic krill eggs hatch in the aphotic zone up to 1000 m depth and larvae develop on their way to the ocean surface (development ascent) and are exposed to different quality (wavelength) and quantity (irradiance) of light. Adults show a daily vertical migration pattern, moving downward during the day and upward during the night within the top 200 m of the water column. Seawater acts as a potent chromatic filter and animals have evolved different opsin photopigments to perceive photons of specific wavelengths. We have investigated the transcriptome of E. superba and, using a candidate gene approach, we identified six novel opsins. Five are r-type visual opsins: four middle-wavelength-sensitive (EsRh2, EsRh3, EsRh4 and EsRh5) and one long-wavelengthsensitive (EsRh6). Moreover, we have identified a non-visual opsin, the EsPeropsin. All these newly identified opsin genes were significantly expressed in compound eyes and brain, while only EsPeropsin and EsRh2 were clearly detected also in the abdomen. A temporal modulation in the transcription of these novel opsins was found, but statistically significant oscillations were only observed in EsRrh3 and EsPeropsin. Our results contribute to the dissection of the complex photoreception system of E. superba, which enables this species to respond to the daily and seasonal changes in irradiance and spectral composition in the Southern Ocean.

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“…The presence of one visual r-opsin in onychophorans and tardigrades (Hering et al 2012;Hering and Mayer 2014) leads to the assumption that monochromatic vision is an ancestral feature of all panarthropods and that colour vision most likely evolved within the arthropod lineage, where the r-opsins are highly diverse ( Fig. 10d; e.g., Briscoe 2000;Porter et al 2007;Koyanagi et al 2008;Kashiyama et al 2009;Katti et al 2010;Battelle et al 2015;Henze and Oakley 2015). Indeed, electrophysiological and behavioural experiments on onychophorans confirm a single peak in the visible light spectrum around 480 nm (blue-green light) and therefore support the hypothesis of monochromatic vision in these animals (Beckmann et al 2015).…”

Section: Evolution Of Visual Organs In Panarthropodsmentioning

confidence: 99%

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

et al. 2017

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Understanding the origin and evolution of arthropods requires examining their closest outgroups, the tardigrades (water bears) and onychophorans (velvet worms). Despite the rise of molecular techniques, the phylogenetic positions of tardigrades and onychophorans in the panarthropod tree (onychophorans + tardigrades + arthropods) remain unresolved. Hence, these methods alone are currently insufficient for clarifying the panarthropod topology. Therefore, the evolution of different morphological traits, such as one of the most intriguing features of panarthropods-their nervous system-becomes essential for shedding light on the origin and evolution of arthropods and their relatives within the Panarthropoda. In this review, we summarise current knowledge of the evolution of panarthropod nervous and visual systems. In particular, we focus on the evolution of segmental ganglia, the segmental identity of brain regions, and the visual system from morphological and developmental perspectives. In so doing, we address some of the many controversies surrounding these topics, such as the homology of the onychophoran eyes to those of arthropods as well as the segmentation of the tardigrade brain. Finally, we attempt to reconstruct the most likely state of these systems in the last common ancestors of arthropods and panarthropods based on what is currently known about tardigrades and onychophorans.

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Opsins inLimuluseyes: Characterization of three visible light-sensitive opsins unique to and co-expressed in median eye photoreceptors and a peropsin/RGR that is expressed in all eyes

Cited by 13 publications

References 81 publications

Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum

Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum

The opsin repertoire of the Antarctic krill Euphausia superba

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

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