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      The planarian TRPA1 homolog mediates extraocular behavioral responses to near-ultraviolet light

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          ABSTRACT

          Although light is most commonly thought of as a visual cue, many animals possess mechanisms to detect light outside of the eye for various functions, including predator avoidance, circadian rhythms, phototaxis and migration. Here we confirm that planarians (like Caenorhabditis elegans, leeches and Drosophila larvae) are capable of detecting and responding to light using extraocular photoreception. We found that, when either eyeless or decapitated worms were exposed to near-ultraviolet (near-UV) light, intense wild-type photophobic behaviors were still observed. Our data also revealed that behavioral responses to green wavelengths were mediated by ocular mechanisms, whereas near-UV responses were driven by extraocular mechanisms. As part of a candidate screen to uncover the genetic basis of extraocular photoreception in the planarian species Schmidtea mediterranea, we identified a potential role for a homolog of the transient receptor potential channel A1 ( TRPA1) in mediating behavioral responses to extraocular light cues. RNA interference (RNAi) to Smed-TrpA resulted in worms that lacked extraocular photophobic responses to near-UV light, a mechanism previously only identified in Drosophila. These data show that the planarian TRPA1 homolog is required for planarian extraocular-light avoidance and may represent a potential ancestral function of this gene. TRPA1 is an evolutionarily conserved detector of temperature and chemical irritants, including reactive oxygen species that are byproducts of UV-light exposure. Our results suggest that planarians possess extraocular photoreception and display an unconventional TRPA1-mediated photophobic response to near-UV light.

          Abstract

          Summary: Planarians use a non-traditional TRPA1-mediated mechanism for extraocular photoresponses to near-UV light, a response previously identified only in Drosophila.

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          Most cited references66

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          The cryptochromes: blue light photoreceptors in plants and animals.

          Cryptochromes are flavoprotein photoreceptors first identified in Arabidopsis thaliana, where they play key roles in growth and development. Subsequently identified in prokaryotes, archaea, and many eukaryotes, cryptochromes function in the animal circadian clock and are proposed as magnetoreceptors in migratory birds. Cryptochromes are closely structurally related to photolyases, evolutionarily ancient flavoproteins that catalyze light-dependent DNA repair. Here, we review the structural, photochemical, and molecular properties of cry-DASH, plant, and animal cryptochromes in relation to biological signaling mechanisms and uncover common features that may contribute to better understanding the function of cryptochromes in diverse systems including in man.
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            UV-induced DNA damage and repair: a review.

            Increases in ultraviolet radiation at the Earth's surface due to the depletion of the stratospheric ozone layer have recently fuelled interest in the mechanisms of various effects it might have on organisms. DNA is certainly one of the key targets for UV-induced damage in a variety of organisms ranging from bacteria to humans. UV radiation induces two of the most abundant mutagenic and cytotoxic DNA lesions such as cyclobutane-pyrimidine dimers (CPDs) and 6-4 photoproducts (6-4PPs) and their Dewar valence Isomers. However, cells have developed a number of repair or tolerance mechanism to counteract the DNA damage caused by UV or any other stressors. Photoreactivation with the help of the enzyme photolyase is one of the most important and frequently occurring repair mechanisms in a variety of organisms. Excision repair, which can be distinguished into base excision repair (BER) and nucleotide excision repair (NER), also plays an important role in DNA repair in several organisms with the help of a number of glycosylases and polymerases, respectively. In addition, mechanisms such as mutagenic repair or dimer bypass, recombinational repair, cell-cycle checkpoints, apoptosis and certain alternative repair pathways are also operative in various organisms. This review deals with UV-induced DNA damage and the associated repair mechanisms as well as methods of detecting DNA damage and its future perspectives.
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              Cryptochrome mediates light-dependent magnetosensitivity in Drosophila.

              Although many animals use the Earth's magnetic field for orientation and navigation, the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors. However, the specific photoreceptor involved in such magnetoreception has not been demonstrated conclusively in any animal. Here we show that the ultraviolet-A/blue-light photoreceptor cryptochrome (Cry) is necessary for light-dependent magnetosensitive responses in Drosophila melanogaster. In a binary-choice behavioural assay for magnetosensitivity, wild-type flies show significant naive and trained responses to a magnetic field under full-spectrum light ( approximately 300-700 nm) but do not respond to the field when wavelengths in the Cry-sensitive, ultraviolet-A/blue-light part of the spectrum (<420 nm) are blocked. Notably, Cry-deficient cry(0) and cry(b) flies do not show either naive or trained responses to a magnetic field under full-spectrum light. Moreover, Cry-dependent magnetosensitivity does not require a functioning circadian clock. Our work provides, to our knowledge, the first genetic evidence for a Cry-based magnetosensitive system in any animal.
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                Author and article information

                Journal
                J Exp Biol
                J. Exp. Biol
                JEB
                jexbio
                The Journal of Experimental Biology
                The Company of Biologists Ltd
                0022-0949
                1477-9145
                15 July 2017
                15 July 2017
                : 220
                : 14
                : 2616-2625
                Affiliations
                Department of Biological Sciences, Western Michigan University , 1903 W. Michigan Avenue, Kalamazoo, MI 49008, USA
                Author notes
                [* ]Author for correspondence ( wendy.beane@ 123456wmich.edu )
                Author information
                http://orcid.org/0000-0002-3762-1025
                Article
                JEB152298
                10.1242/jeb.152298
                5536891
                28495872
                d3f7e945-6990-42a2-be35-1a35777dd13b
                © 2017. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 26 October 2016
                : 4 May 2017
                Funding
                Funded by: Western Michigan University, http://dx.doi.org/10.13039/100007159;
                Categories
                Research Article

                Molecular biology
                planaria,extraocular photoreception,dermal phototransduction,uv-light detection,trpa1,neuroethology

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