Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin

Rivera, Ajna S.; Öztürk, Nuri; Fahey, Bryony; Plachetzki, David C.; Degnan, Bernard M.; Sancar, Aziz; Oakley, Todd H.

doi:10.1242/jeb.067140

Cited by 99 publications

(146 citation statements)

References 67 publications

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“…Neither an opsin nor an MLT receptor could be identified in Oscarella and Amphimedon, and we can thus conclude that both these protein families are eumetazoan specific. This confirms recent results showing that light sensitivity in Amphimedon is mediated by a cryptochrome, rather than an opsin (28). Fig.…”

Section: Resultssupporting

confidence: 92%

Metazoan opsin evolution reveals a simple route to animal vision

Feuda

Hamilton

McInerney

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

173

212

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The authors wish to note the following: "The contrast of our final projection map was inverted, so that we interpreted the background density rather than the actual protein density in terms of structural features of the potassium channel-Fv complex. In addition, we indexed the 2D crystals with unit cell parameters of a = b = 175 Å, while the correct indexing would be a = b = 124 Å. Given these analysis errors, the resulting density map and our interpretation of the structural features are not correct. Accordingly, we would like to retract this paper. We acknowledge Yoshinori Fujiyoshi, Rod MacKinnon, Kazutoshi Tani, and Tom Walz for identifying the errors and pointing them out to us."

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Section: Resultssupporting

confidence: 92%

Metazoan opsin evolution reveals a simple route to animal vision

Feuda

Hamilton

McInerney

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

173

212

View full text Add to dashboard Cite

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“…Parallel to this process, the membrane-bound cryptochrome is associated with NOSIP, suggesting that the cryptochrome pathway is coupled to the NO synthase signaling cascade. As initially described by us ) and subsequently confirmed (Rivera et al 2012), light response of the sponge cryptochrome results in a photoreduction, the photoresponsiveness of the flavoprotein, under formation of FADH 2 (reduced flavin adenine dinucleotide) from flavin adenine dinucleotide (FAD (Weber et al 2010;Müller and Ahmad 2011). Essentially, this reaction also takes place in the modular eukaryotic NOS isoforms that are composed of (1) the C-terminal reductase domain that binds reduced nicotinamide adenine dinucleotide phosphate (NADPH), flavin mononucleotide (FMN), and FAD and (2) the N-terminal oxygenase domain (see Förstermann and Münzel 2006).…”

Section: Introductionsupporting

confidence: 70%

“…From earlier studies with sponge systems, it is known that cryptochrome is an inducible gene Rivera et al 2012). The same property has been described for the mammalian NOSIP (Yu et al 2012).…”

Section: Discussionmentioning

confidence: 52%

“…Likewise, the master control gene, Pax6, for eye development in bilateria (Gehring and Seimiya 2010), has not been found in sponges. In turn, we proposed that, in sponges, the cryptochrome represents the (major) photoreceptive system ), a finding that has been corroborated recently in the sponge A. queenslandica (Rivera et al 2012). The experimental data gathered indicate that it is blue light that is most sensitively perceived by the cryptochrome system; this light spectral range is generated by the sponge luciferase system (Müller et al 2009) and also exists in the marine twilight zone, where sponges live.…”

Section: Introductionmentioning

confidence: 65%

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Cryptochrome in Sponges

Müller

Schröder

Markl

et al. 2013

J Histochem Cytochem.

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SummarySponges (phylum: Porifera) react to external light or mechanical signals with contractile or metabolic reactions and are devoid of any nervous or muscular system. Furthermore, elements of a photoreception/phototransduction system exist in those animals. Recently, a cryptochrome-based photoreceptor system has been discovered in the demosponge. The assumption that in sponges the siliceous skeleton acts as a substitution for the lack of a nervous system and allows light signals to be transmitted through its glass fiber network is supported by the findings that the first spicules are efficient light waveguides and the second sponges have the enzymatic machinery for the generation of light. Now, we have identified/ cloned in Suberites domuncula two additional potential molecules of the sponge cryptochrome photoreception system, the guanine nucleotide-binding protein β subunit, related to β-transducin, and the nitric oxide synthase (NOS)-interacting protein. Cryptochrome and NOSIP are light-inducible genes. The studies show that the NOS inhibitor L-NMMA impairs both morphogenesis and motility of the cells. Finally, we report that the function of primmorphs to produce reactive nitrogen species can be abolished by a NOS inhibitor. We propose that the sponge cryptochrome-based photoreception system, through which photon signals are converted into radicals, is coupled to the NOS apparatus. ( J Histochem Cytochem 61:814-832, 2013)

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“…As A. queenslandica is a representative of one of the oldest extant animal phyletic lineages (Porifera), those components of a sponge circadian clock that are shared with eumetazoans are likely to reflect a core clock present in the last common animal ancestor. It already has been reported that the A. queenslandica genome encodes two cryptochrome genes, at least one of which appears to drive photic behaviors in the larva (Rivera et al, 2012), as well as a suite of conserved bHLH-PAS and bZIPs transcription factors (Simionato et al, 2007;Jindrich and Degnan, 2016). Here, we report on the presence or absence of the remaining putative animal circadian genes in the A. queenslandica genome, so as to provide the first comprehensive list of circadian gene orthologs in a sponge.…”

Section: Introductionmentioning

confidence: 91%

Origin of the Animal Circadian Clock: Diurnal and Light-Entrained Gene Expression in the Sponge Amphimedon queenslandica

et al. 2017

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The circadian clock is a molecular network that coordinates organismal behavior and physiology with daily environmental changes in the day-night cycle. In eumetazoans (bilaterians + cnidarians), this network appears to be largely conserved, yet different from other known eukaryotic circadian networks. To determine if the eumetazoan circadian network has an older origin, we ask here whether orthologs comprising this network are expressed in a manner consistent with a role in regulating circadian patterns in a representative of an earlier-branching animal lineage, the sponge Amphimedon queenslandica. The A. queenslandica genome encodes orthologs of many eumetazoan circadian genes, including two cryptochrome genes that encode flavoproteins, three Timeout genes, and two PAR-bZIP and seven bHLH-PAS transcription factor genes.There is no apparent Cycle ortholog, although we can identify three closely related ARNT genes. Of the putative circadian genes, only AqPARa and AqCry2 have a consistent oscillating diurnal expression profile, and the rhythmic expression of both these genes is partially lost when the animals are exposed to constant light or darkness. Expression of the other putative circadian genes, in particular AqClock, is neither diurnally-oscillating nor light-dependent. AqPARa and AqCry2 are also temporally and spatially co-expressed throughout embryonic and larval development. Transcripts of these genes are enriched first in cells comprising the larval posterior pigment ring, which is a simple photosensory organ that is responsible for the negative phototactic behavior displayed by larvae, and subsequently in the larval epithelial and subepithelial layers. The combined findings of no clear Cycle ortholog and of PAR-bZIP and cryptochrome being the only orthologs expressed in a pattern consistent with a circadian role suggests that either (i) the ancestral metazoan circadian network was simpler than the eumetazoan network, or (ii) that this sponge has lost some components, as has occurred in some other animals such as Hydra.

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Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin

Cited by 99 publications

References 67 publications

Metazoan opsin evolution reveals a simple route to animal vision

Metazoan opsin evolution reveals a simple route to animal vision

Cryptochrome in Sponges

Origin of the Animal Circadian Clock: Diurnal and Light-Entrained Gene Expression in the Sponge Amphimedon queenslandica

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