High opsin diversity in a non-visual infaunal brittle star

BMC Genomics

Patrick Flammang⁵  Jérôme Mallefet¹  Maria-Ina Arnone²  Sam Dupont³  Olga Ortega-Martinez³  Esther Ullrich-Lüter⁴  Jérôme Delroisse⁵ 

[1] Laboratory of Marine Biology, Earth and Life Institute, Catholic University of Louvain, Louvain-La-Neuve, Place Croix du Sud 3, bt L7.06.04, 1348 Louvain-la-Neuve, Belgium;Stazione Zoologica Anton Dohrn, Cellular and Developmental Biology, Villa Comunale, 80121, Naples, Italy;Department of Biological and Environmental Science, The Sven Lovén Centre for Marine Sciences – Kristineberg, University of Gothenburg, 45178 Fiskebäckskil, Sweden;Museum für Naturkunde, Invalidenstr. 43, 10115 Berlin, Germany;Biology of Marine Organisms and Biomimetics, Research Institute for Biosciences, University of Mons, Avenue du Champs de Mars 6, 7000 Mons, Belgium

关键词: Transcriptome;    Genome;    Photoreception;    Ophiuroidea;    Echinodermata;    Opsin;   

Others  :  1090523
DOI  :  10.1186/1471-2164-15-1035

 received in 2014-07-22, accepted in 2014-11-19,  发布年份 2014

【 摘 要 】

Background

In metazoans, opsins are photosensitive proteins involved in both vision and non-visual photoreception. Echinoderms have no well-defined eyes but several opsin genes were found in the purple sea urchin (Strongylocentrotus purpuratus) genome. Molecular data are lacking for other echinoderm classes although many species are known to be light sensitive.

Results

In this study focused on the European brittle star Amphiura filiformis, we first highlighted a blue-green light sensitivity using a behavioural approach. We then identified 13 new putative opsin genes against eight bona fide opsin genes in the genome of S. purpuratus. Six opsins were included in the rhabdomeric opsin group (r-opsins). In addition, one putative ciliary opsin (c-opsin), showing high similarity with the c-opsin of S. purpuratus (Sp-opsin 1), one Go opsin similar to Sp-opsins 3.1 and 3.2, two basal-branch opsins similar to Sp-opsins 2 and 5, and two neuropsins similar to Sp-opsin 8, were identified. Finally, two sequences from one putative RGR opsin similar to Sp-opsin 7 were also detected. Adult arm transcriptome analysis pinpointed opsin mRNAs corresponding to one r-opsin, one neuropsin and the homologue of Sp-opsin 2. Opsin phylogeny was determined by maximum likelihood and Bayesian analyses. Using antibodies designed against c- and r-opsins from S. purpuratus, we detected putative photoreceptor cells mainly in spines and tube feet of A. filiformis, respectively. The r-opsin expression pattern is similar to the one reported in S. purpuratus with cells labelled at the tip and at the base of the tube feet. In addition, r-opsin positive cells were also identified in the radial nerve of the arm. C-opsins positive cells, expressed in pedicellariae, spines, tube feet and epidermis in S. purpuratus were observed at the level of the spine stroma in the brittle star.

Conclusion

Light perception in A. filiformis seems to be mediated by opsins (c- and r-) in, at least, spines, tube feet and in the radial nerve cord. Other non-visual opsin types could participate to the light perception process indicating a complex expression pattern of opsins in this infaunal brittle star.

【 授权许可】

   
2014 Delroisse et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Land MF, Fernald RD: The evolution of eyes. Annu Rev Neurosci 1992, 15:1-29.
• [2]Nilsson D-E: Eye evolution: a question of genetic promiscuity. Curr Opin Neurobiol 2004, 14:407-414.
• [3]Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD: The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952.
• [4]Raible F, Tessmar-Raible K, Arboleda E, Kaller T, Bork P, Arendt D, Arnone MI: Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Dev Biol 2006, 300:461-475.
• [5]Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T, Liang S, Mu X, Agca C, Klein WH: A genomic view of the sea urchin nervous system. Dev Biol 2006, 300:434-460.
• [6]Lesser MP, Carleton KL, Böttger SA, Barry TM, Walker CW: Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. P Roy Soc B-Biol Sci 2011, 278:3371-3379.
• [7]Ooka S, Katow T, Yaguchi S, Yaguchi J, Katow H: Spatiotemporal expression pattern of an encephalopsin orthologue of the sea urchin Hemicentrotus pulcherrimus during early development, and its potential role in larval vertical migration. Develop Growth Differ 2010, 52:195-207.
• [8]Agca C, Elhajj MC, Klein WH, Venuti JM: Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus. J Comp Neurol 2011, 519:3566-3579.
• [9]Ullrich-Lüter EM, Dupont S, Arboleda E, Hausen H, Arnone MI: Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci U S A 2011, 108:8367-8372.
• [10]Ullrich-Lüter EM, D’Aniello S, Arnone MI: C-opsin expressing photoreceptors in echinoderms. Am Zool 2013, 53:27-38.
• [11]Land MF, Nilsson D-E: Animals Eyes. 2002.
• [12]Hendler G: An echinoderm’s Eye View of Photoreception and Vision. 2006, 339.
• [13]Oviatt CA: Light influenced movement of the starfish AsterIas forbesi (Desor). Behaviour 1969, 33:1-2.
• [14]Millott N: The photosensitivity of echinoids. Adv Mar Biol 1976, 13:1-52.
• [15]Yerramilli D, Johnsen S: Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). J Exp Biol 2010, 213:249-255.
• [16]Yoshida M, Ohtsuki H: Compound ocellus of a starfish: its function. Science 1966, 153:197-198.
• [17]Hendler G, Byrne M: Fine structure of the dorsal arm plate of Ophiocoma wendti: evidence for a photoreceptor system (Echinodermata, Ophiuroidea). Zoomorphology 1987, 107:261-272.
• [18]Garm A, Nilsson D-E: Visual navigation in starfish: first evidence for the use of vision and eyes in starfish. Proc R Soc B Biol Sci 2014, 281:20133011.
• [19]Yamamoto M, Yoshida M: Fine structure of the ocelli of a synaptid holothurian, Opheodesoma spectabilis, and the effects of light and darkness. Zoomorphologie 1978, 90:1-17.
• [20]Berrill M: The ethology of the synaptid holothurian, Opheodesoma spectabilis. Can J Zool 1966, 44:457-482.
• [21]Smith JE: On the nervous system of the starfish Marthasterias glacialis (L.). Philos T Roy Soc B 1937, 227:111-173.
• [22]Eakin RM, Brandenburger JL: Effects of light on ocelli of seastars. Zoomorphologie 1979, 92:191-200.
• [23]Penn PE, Alexander CG: Fine structure of the optic cushion in the asteroid Nepanthia belcheri. Mar Biol 1980, 58:251-256.
• [24]Takasu N, Yoshida M: Photic effects on photosensory microvilli in the seastar Asterias amurensis (Echinodermata: Asteroida). Zoomorphology 1983, 103:135-148.
• [25]Johnsen S: Identification and localization of a possible rhodopsin in the echinoderms Asterias forbesi (Asteroidea) and Ophioderma brevispinum (Ophiuroidea). Biol Bull 1997, 193:97-105.
• [26]Delroisse J, Lanterbecq D, Eeckhaut I, Mallefet J, Flammang P: Opsin detection in the sea urchin Paracentrotus lividus and the sea star Asterias rubens. Cah Biol Mar 2013, 54:721-727.
• [27]Yoshida M: Extraocular Photoreception. In Comparative Physiology and Evolution of Vision in Invertebrates Edited by Springer Berlin Heidelberg. 1979, 581-640.
• [28]Yoshida M, Takasu N, Tamotsu S: Photoreception in Echinoderms. In Photoreception and Vision in Invertebrates. Edited by Ali MA. US: Springer; 1984:743-771.
• [29]Yoshida M, Ohtsuki H: The phototactic behavior of the starfish, Asterias amurensis Lütken. Biol Bull 1968, 134:516-532.
• [30]Cobb JL, Moore A: Comparative studies on receptor structure in the brittlestar Ophiura ophiura. J Neurocytol 1986, 15:97-108.
• [31]Aizenberg J, Tkachenko A, Weiner S, Addadi L, Hendler G: Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 2001, 412:819-822.
• [32]Rosenberg R: Benthic marine fauna structured by hydrodynamic processes and food availability. Neth J Sea Res 1995, 34:303-317.
• [33]Josefson AB: Large-scale estimate of somatic growth in Amphiura filiformis (Echinodermata: Ophiuroidea). Mar Biol 1995, 124:435-442.
• [34]Baden SP, Pihl L, Rosenberg R: Effects of oxygen depletion on the ecology, blood physiology and fishery of the Norway lobster Nephrops norvegicus. Mar Ecol Prog Ser 1990, 67:141-155.
• [35]Duineveld G, Van Noort GJ: Observations on the population dynamics of Amphiura filiformis (Ophiuroidea: Echinodermata) in the southern North Sea and its exploitation by the dab, Limanda limanda. Neth J Sea Res 1986, 20:85-94.
• [36]Pihl L: Changes in the diet of demersal fish due to eutrophication-induced hypoxia in the Kattegat, Sweden. Can J Fish Aquat Sci 1994, 51:321-336.
• [37]Woodley JD: The behaviour of some amphiurid Brittle stars. J Exp Mar Biol Ecol 1975, 18:29-46.
• [38]Loo L-O, Rosenberg R: Production and energy budget in marine suspension feeding populations: Mytilus edulis, Cerastoderma edule, Mya arenaria and Amphiura filiformis. J Sea Res 1996, 35:199-207.
• [39]Solan M, Kennedy R: Observation and quantification of in situ animal-sediment relations using time-lapse sediment profile imagery (t-SPI). Mar Ecol-Progr Ser 2002, 228:179-191.
• [40]Rosenberg R, Lundberg L: Photoperiodic activity pattern in the brittle star Amphiura filiformis. Mar Biol 2004, 145:651-656.
• [41]Burns G, Ortega-Martinez O, Thorndyke MC, Peck LS, Dupont S, Clark MS: Dynamic gene expression profiles during arm regeneration in the brittle star Amphiura filiformis. J Exp Mar Biol Ecol 2011, 407:315-322.
• [42]Burns G, Ortega-Martinez O, Dupont S, Thorndyke MC, Peck LS, Clark MS: Intrinsic gene expression during regeneration in arm explants of Amphiura filiformis. J Exp Mar Biol Ecol 2012, 413(C):106-112.
• [43]Czarkwiani A, Dylus DV, Oliveri P: Expression of skeletogenic genes during arm regeneration in the brittle star Amphiura filiformis. Gene Expr Patterns 2013, 13:464-472.
• [44]Pearson WR, Wood T, Zhang Z, Miller W: Comparison of DNA sequences with protein sequences. Genomics 1997, 46:24-36.
• [45]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [46]Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A: Protein Identification and Analysis Tools on the ExPASy Server. 2005, 571-607.
• [47]Burge CB, Karlin S: Finding the genes in genomic DNA. Curr Opin Struct Biol 1998, 8:346-354.
• [48]Jones DT, Taylor WR, Thornton JM: A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 1994, 33:3038-3049.
• [49]Gouy M, Guindon S, Gascuel O: SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224.
• [50]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [51]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
• [52]Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9:299-306.
• [53]Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, Strnad H, Kawamura S, Piatigorsky J, Paces V: Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci U S A 2008, 105:8989-8993.
• [54]Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T, Cronin TW, Robinson PR: Shedding new light on opsin evolution. P Roy Soc B-Biol Sci 2012, 279:3-14.
• [55]Feuda R, Hamilton SC, McInerney JO, Pisani D: Metazoan opsin evolution reveals a simple route to animal vision. Proc Natl Acad Sci U S A 2012, 109:18868-18872.
• [56]Feuda R, Rota-Stabelli O, Oakley TH, Pisani D: The Comb Jelly Opsins and the origins of animal phototransduction. Genome Biol Evol 2014, 6:1964-1971.
• [57]Guindon S, Delsuc F, Dufayard J-F, Gascuel O: Estimating Maximum Likelihood Phylogenies with PhyML. 2009, 113-137.
• [58]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [59]Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 18:691-699.
• [60]Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012, 61:539-542.
• [61]Shichida Y: Evolution of opsins and phototransduction. Philos T R Soc B 2009, 364:2881-2895.
• [62]Terakita A, Kawano-Yamashita E, Koyanagi M: Evolution and diversity of opsins. WIREs Membr Transp Signal 2012, 1:104-111.
• [63]Terakita A, Koyanagi M, Tsukamoto H, Yamashita T, Miyata T, Shichida Y: Counterion displacement in the molecular evolution of the rhodopsin family. Nat Struct Mol Biol 2004, 11:284-289.
• [64]Bockaert J, Philippe Pin J: Molecular tinkering of G protein‒coupled receptors: an evolutionary success. EMBO J 1999, 18:1723-1729.
• [65]Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE: Crystal structure of rhodopsin: AG protein-coupled receptor. Science 2000, 289:739-745.
• [66]Fritze O, Filipek S, Kuksa V, Palczewski K, Hofmann KP, Ernst OP: Role of the conserved NPxxY (x) 5, 6F motif in the rhodopsin ground state and during activation. Proc Natl Acad Sci U S A 2003, 100:2290-2295.
• [67]Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J: Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004, 306:869-871.
• [68]Mooi R, David B: What a new model of skeletal homologies tells us about asteroid evolution. Am Zool 2000, 40:326-339.
• [69]Littlewood D, Smith AB, Clough KA, Emson RH: The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol J Linn Soc 1997, 61:409-438.
• [70]Smith MJ, Arndt A, Gorski S, Fajber E: The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 1993, 36:545-554.
• [71]Telford MJ, Lowe CJ, Cameron CB, Ortega-Martinez O, Aronowicz J, Oliveri P, Copley RR: Phylogenomic analysis of echinoderm class relationships supports Asterozoa. Proc Biol Sci 2014, 281:20140479.
• [72]Hendler G: Brittlestar color-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Mar Ecol 1984, 5:379-401.
• [73]Giese AC, Farman-Farmanian A: Resistance of the purple sea urchin to osmotic stress. Biol Bull 1963, 124:182-192.
• [74]McFarland W: Light in the sea: the optical world of elasmobranchs. J Exp Zool 1990, 256:3-12.
• [75]Claes JM, Aksnes DL, Mallefet J: Phantom hunter of the fjords: camouflage by counterillumination in a shark (Etmopterus spinax). J Exp Mar Biol Ecol 2010, 388:28-32.
• [76]Herring PJ: New observations on the bioluminescence of echinoderms. J Zool 1974, 172:401-418.
• [77]Delroisse J, Flammang P, Mallefet J: Marine luciferases: are they really species-specific? A putative luciferase evolved by co-option in an echinoderm lineage. In Proceedings of the 18th International Symposium on Bioluminescence and Chemiluminescence. Edited by Kricka LJ. Uppsala; 2014.
• [78]Solan M, Battle EJ: Does the ophiuroid Amphiura filiformis alert conspecifics to the danger of predation through the generation of an alarm signal? J Mar Biol Ass 2003, 83:1117-1118.
• [79]Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ: Evidence for light perception in a bioluminescent organ. Proc Natl Acad Sci U S A 2009, 106:9836-9841.
• [80]Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan JF, Simmons D, Tada T, Park M, Gupta J, Brooks SY: Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol 2012, 10:107. BioMed Central Full Text
• [81]Mallefet J: Echinoderm bioluminescence: where, how and why do so many ophiuroids glow? In Bioluminescence in Focus – A Collection of Illuminating Essays. Edited by Meyer-Rochow VB. Trivandrum: Research signpost; 2009:67-83.
• [82]Kumbalasiri T, Provencio I: Melanopsin and other novel mammalian opsins. Exp Eye Res 2005, 81:368-375.
• [83]Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, O’Hara BF: Role of melanopsin in circadian responses to light. Science 2002, 298:2211-2213.
• [84]Nasi E, Del Pilar Gomez M: Melanopsin-mediated light-sensing in amphioxus. Commun Integr Biol 2009, 2(5):441-443.
• [85]Shichida Y, Yamashita T, Imai H, Kishida T: Evolution and Senses: Opsins, Bitter Taste, and Olfaction. 2013.
• [86]Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG: Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice. Nature 2003, 424:75-81.
• [87]Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M: Melanopsin is required for non-image-forming photic responses in blind mice. Science 2003, 301:525-527.
• [88]Koyanagi M, Terakita A: Gq-coupled Rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem Photobiol 2008, 84:1024-1030.
• [89]Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, Schmedt C, Jegla T, Panda S: Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE 2008, 3:e2451.
• [90]Plachetzki DC, Serb JM, Oakley TH: New insights into the evolutionary history of photoreceptor cells. Trends Ecol Evol 2005, 20:465-467.
• [91]Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD: A novel human opsin in the inner retina. J Neurosci 2000, 20:600-605.
• [92]Hattar S, Liao H-W, Takao M, Berson DM, Yau K-W: Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 2002, 295:1065-1070.
• [93]Rollag MD, Berson DM, Provencio I: Melanopsin, ganglion-cell photoreceptors, and mammalian photoentrainment. J Biol Rhythm 2003, 18:227-234.
• [94]Fu Y, Zhong H, Wang M-HH, Luo D-G, Liao H-W, Maeda H, Hattar S, Frishman LJ, Yau K-W: Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc Natl Acad Sci U S A 2005, 102:10339-10344.
• [95]Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, Tarttelin EE, Iuvone PM, Hankins MW, Tosini G, Lucas RJ: Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. Plos Biol 2006, 4:e254.
• [96]Brandenburger JL, Woolacott RM, Eakin RM: Fine structure of eyespots in tornarian larvae (Phylum: Hemichordata). Z Zellforsch Mikrosk Anat 1973, 142:89-102.
• [97]Nezlin LP, Yushin VV: Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology 2004, 123:1-13.
• [98]Fain GL, Hardie R, Laughlin SB: Phototransduction and the evolution of photoreceptors. Curr Biol 2010, 20:R114-R124.
• [99]Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez È, Blow MJ, Bronner-Fraser M, Brunet F, Butts T, Candiani S, Dishaw LJ: The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 2008, 18:1100-1111.
• [100]Kusakabe T, Tsuda M: Photoreceptive systems in ascidians. Photochem Photobiol 2007, 83:248-252.
• [101]Tarttelin EE, Bellingham J, Hankins MW, Foster RG, Lucas RJ: Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Lett 2003, 554:410-416.
• [102]Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y: Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci U S A 2010, 107:22084-22089.
• [103]Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y: UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS ONE 2011, 6:e26388.
• [104]Frank TM, Johnsen S, Cronin TW: Light and vision in the deep-sea benthos: II. Vision in deep-sea crustaceans. J Exp Biol 2012, 215:3344-3353.
• [105]Buchanan JB: Mucus secretion within the spines of ophiuroid echinoderms. Proc Zool Soc London 1963, 141:251-259.
• [106]Arendt D, Hausen H, Purschke G: The “division of labour” model of eye evolution. Philos T R Soc B 2009, 364:2809-2817.
• [107]Nilsson D-E: The evolution of eyes and visually guided behaviour. Philos T Roy Soc B 2009, 364:2833-2847.
• [108]Morris VB, Selvakumaraswamy P, Whan R, Byrne M: Development of the five primary podia from the coeloms of a sea star larva: homology with the echinoid echinoderms and other deuterostomes. P Roy Soc B-Biol Sci 2009, 276:1277-1284.
• [109]Takahashi K: Electrical responses to light stimuli in the isolated radial nerve of the sea urchin, Diadema setosum (Leske). Nature 1964, 201:1343-1344.
• [110]Millott N: Sensitivity to light and the reactions to changes in light intensity of the echinoid Diadema antillarum Philippi. Philos T R Soc B 1954, 238:187-220.
• [111]Cobb J, Stubbs TR: The giant neurone system in ophiuroids. Cell Tissue Res 1981, 219:197-207.
• [112]Stubbs TR: The Neurophysiology of Photosensitivity in Ophiuroids. 1982, 403-408.
• [113]Moore A, Cobb J: Neurophysiological studies on photic responses in Ophiura ophiura. Comp Biochem Phys A 1985, 80:11-16.
• [114]Wolken JJ: Photobehavior of marine invertebrates: extraocular photoreception. Comp Biochem Phys C 1988, 91:145-149.
• [115]Kartelija G, Nedeljkovic M, Radenovic L: Photosensitive neurons in mollusks. Comp Biochem Phys A 2003, 134:483-495.
• [116]Biressi ACM, Zou T, Dupont S, Dahlberg C, Di Benedetto C, Bonasoro F, Thorndyke M, Carnevali MDC: Wound healing and arm regeneration in Ophioderma longicaudum and Amphiura filiformis (Ophiuroidea, Echinodermata): comparative morphogenesis and histogenesis. Zoomorphology 2010, 129:1-19.
• [117]Delroisse J, Mallefet J, Flammang P: Raw sequencing reads (Amphiura filiformis, adult arm tissues). [NCBI SRA repository] [http://www.ncbi.nlm.nih.gov/sra/?term=SRR1523743 webcite]
• [118]Delroisse J, Ullrich-Lüter E, Ortega-Martinez O, Dupont S, Arnone M, Mallefet J, Flammang P: Truncated opsin alignment. [DRYAD Data repository] [http://dx.doi.org/10.5061/dryad.7s8h7 webcite]
• [119]Delroisse J, Ullrich-Lüter E, Ortega-Martinez O, Dupont S, Arnone M, Mallefet J, Flammang P: ML tree. [DRYAD Data repository] [http://dx.doi.org/10.5061/dryad.7s8h7 webcite]
• [120]Delroisse J, Ullrich-Lüter E, Ortega-Martinez O, Dupont S, Arnone M, Mallefet J, Flammang P: Bayesian tree. [DRYAD Data repository] [http://dx.doi.org/10.5061/dryad.7s8h7 webcite]