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Amphioxus Photoreceptors - Insights Into the Evolution of Vertebrate Opsins, Vision and Circadian Rhythmicity JIRI PERGNER and ZBYNEK KOZMIK*

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Amphioxus Photoreceptors - Insights Into the Evolution of Vertebrate Opsins, Vision and Circadian Rhythmicity JIRI PERGNER and ZBYNEK KOZMIK* Int. J. Dev. Biol. 61: 665-681 (2017) doi: 10.1387/ijdb.170230zk www.intjdevbiol.com Amphioxus photoreceptors - insights into the evolution of vertebrate opsins, vision and circadian rhythmicity JIRI PERGNER and ZBYNEK KOZMIK* Laboratory of Transcriptional Regulation, Institute of Molecular Genetics of the Czech Academy of Sciences, Prague, Czech Republic, ABSTRACT Studies on amphioxus, representing the most basal group of chordates, can give in- sights into the evolution of vertebrate traits. The present review of amphioxus research is focused on the physiology of light-guided behavior as well as on the fine structure, molecular biology, and electrophysiology of the nervous system, with special attention being given to the photoreceptive organs. The amphioxus visual system is especially interesting because four types of receptors are involved in light detection – dorsal ocelli and Joseph cells (both rhabdomeric photoreceptors) and the frontal eye and lamellar body (both ciliary photoreceptors). Here, we consider how the available information on photoreceptive organs and light-guided behavior in amphioxus helps generate hy- potheses about the history of these features during chordate and subsequently vertebrate evolution. KEY WORDS: chordate, opsin evolution, photoreceptor, eye evolution, phototransduction Introduction as a valuable model providing useful insight into photoreception in ancestral chordates as well as into evolution of the vertebrate Light is a crucial environmental signal for most of the organ- eye. Cephalochordates (common name amphioxus or lancelets) isms on earth. Light sensing systems have evolved to be uniquely represent the most basal branch of chordates (which also includes suited to the environment and behavior of any given species. vertebrates), live worldwide in sandy shallow seashores and can Light cues are necessary for mediating biological processes such be divided into three genera, Asymmetron, Branchiostoma, and as circadian rhythms, reproductive cycles and most importantly Epigonichthys (Bertrand and Escriva, 2011). visually guided behavior. Animals detect light using sensory cells The amphioxus body plan resembles the body plan of most known as photoreceptors, present in the eyes or, in the case of extant as well as extinct chordates, having a dorsally located extraocular photoreceptors, outside of the eyes. Although other notochord and neural tube, a ventral gut, a perforated pharynx systems of light detection exist in the animal kingdom, such as with gill slits, segmented muscles and gonads and a tail fin. The cryptochromes (Rivera et al., 2012) or LITE-1 (Gong et al., 2016), amphioxus central nervous system comprises a dorsal neural tube opsins, the seven-pass transmembrane proteins that belong to the running through the whole length of the body. The anterior part of G-Protein Coupled Receptor (GPCR) superfamily, are dominantly the neural tube is slightly expanded, forming a so-called cerebral utilized as visual pigments among Metazoa (Feuda et al., 2014). A simple eye can be defined as a photoreceptor cell neighboring a shielding pigment cell, or, in extreme cases, both photoreceptive Abbreviations used in this paper: 2RWGD, two rounds of whole genome duplication; and pigment function can be combined together in one cell. At cAMP, cyclic adenosine monophosphate; cGMP, cyclic guanosine monophosphate; CNG channel, cyclic nucleotide gated channel; CV, cerebral vesicle; DAG, diacyl- the other end of the sophistication spectrum, complex eyes with glycerol; DO, dorsal ocellus; EM, electron microscopical; FE, frontal eye; GNA, advanced optics can be found in various animals. For example the guanine nucleotide-binding protein alpha subunit; GPCR, G protein coupled vertebrate-style camera eye is one of the most elaborate types of receptor; IP3, inositol trisphosphate; ipRGC, intrinsic photosensitive ganglion animal eye. The huge diversity, as well as the extreme complex- cell; JC, Joseph cell; LB, lamellar body; PDE, phosphodiesterase; PIP2, phospha- ity, of eyes in different animals was already puzzling scientists in tidylinositol 4,5-bisphosphate; PKC, protein kinase C; PLC, phospholipase C; Darwin´s time (Darwin, 1859). PMC, primary motor center; PUFA, polyunsaturated fatty acid; RDGN, retinal Recent studies have shown that cephalochordates may serve determination gene network; RPE, retinal pigmented epithelium. *Address correspondence to: Zbynek Kozmik, Institute of Molecular Genetics of the Czech Academy of Sciences, v.v.i., Videnska 1083, 14220, Czech Republic. Tel: +420 241062110. E-mail: [email protected] http://orcid.org/0000-0002-5850-2105 Submitted: 9 September, 2017; Accepted: 22 September, 2017. ISSN: Online 1696-3547, Print 0214-6282 © 2017 UPV/EHU Press (Bilbao, Spain) and Creative Commons CC-BY. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creative- commons.org/licenses/), which permits you to Share (copy and redistribute the material in any medium or format) and Adapt (remix, transform, and build upon the material for any purpose, even commercially), providing you give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use. Printed in Spain 666 J. Pergner and Z. Kozmik vesicle (CV). Based on morphological and molecular analysis, the responses in adult amphioxus (Parker, 1908). Moreover, it was cerebral vesicle is considered to be a homolog of the vertebrate shown that amphioxus adults evince higher burrowing activity diencephalon or di- plus mesencephalon with indistinguishable during the night (Schomerus et al., 2008). Several later studies borders (Albuixech-Crespo et al., 2017; Holland, 2017). added more information about larval amphioxus reactions to light. Amphioxus possesses four distinct photoreceptive organs – the Chin (1941) documented collections of planktonic larvae of Bran- frontal eye (FE), lamellar body (LB), Joseph cells (JCs) and dorsal chiostoma belcheri in different times of the day and night. During ocelli (DO) (Fig. 1). Amphioxus development, from fertilization to the day, amphioxus larvae were found close to the bottom, while metamorphosis, takes about several weeks to several months with decrease in light intensity during sunset, most larvae were depending on species. Amphioxus larvae are planktonic, while after found close to the surface. Comparable observations were made metamorphosis, adult amphioxus spend most of their life burrowed two decades later by Wickstead and Bone (1959), who found an in the sand with just the anterior part of the body projecting outside, increase in concentration of amphioxus larvae close to the surface in order to allow feeding by filtering food particles. Associated with shortly before and after sunset for B. belcheri as well as Branchios- such a dramatic changes in the way of life are also changes in toma lanceolatum. Various amphioxus species thus demonstrate response to light stimuli. typical diurnal migration. Additionally, Webb (1969) showed that amphioxus larvae actively swim to the surface and passively sank Amphioxus responses to light stimuli down, with mouth open, catching food. This behavior is also light dependent. Moreover, it was shown that the FE might be important The rapid reactions of amphioxus to light had been discovered by for larval light guided behavior. During feeding, amphioxus larvae Costa (1834), and thorough study of amphioxus sensory reactions adopt a vertical posture in the water column in such a way that the was performed at the beginning of the 20th century. Parker (1908) FE pigment cells screen off most of light coming towards the FE described sensory reactions of amphioxus to various physical photoreceptor cells (Stokes and Holland, 1995). Larvae are able and chemical stimuli, including light. Parker´s observation about to change their orientation in the order of minutes, when the light amphioxus photoresponses were in agreement with previous direction is changed. Such an orientation to incoming light might be studies (Hesse, 1898; Willey, 1894), showing negative phototactic important for minimizing the overhead illumination and improving the ability to discriminate between levels of light intensity A (Lacalli, 1996). Amphioxus reacts to light as early as the neurula stage. For Branchiostoma floridae it was shown that, when kept in Petri dishes, neurulae swim up to the surface of the water in the direction towards the highest light intensity (Holland and Yu, 2004). No such behavior occurs in the same developmental stage in B. lanceolatum (our observations) or representative of another amphioxus genus Asymmetron lucayanum (Holland and Holland, 2010). Whether light attraction in B. floridae neurula is connected Frontal Lamellar Joseph Dorsal ocelli with ongoing development of the first dorsal ocellus is un- B eye body cells (Hesse organs) clear. Why this phototactic behavior of neurulae was not PRC PRC observed in other amphioxus species remains a mystery. Of special interest is the dependence of amphioxus PRCs PGMC PGMC spawning on light conditions. Branchiostoma species kept in laboratory conditions (B. floridae, B. lanceolatum and PRC B. belcheri) spawn within 1 hour after switching off the light (1h after simulated sunset) (Fuentes et al., 2007; Holland PP and Yu, 2004; Li et al., 2013). Spawning of Branchiostoma M GS shortly after sunset likely occurs in nature as well. The GS same
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