Isolation and characterization of melanopsin photoreceptors of atlantic salmon (<i>Salmo salar</i>)

Sandbakken, Mari; Ebbesson, Lars O.E.; Stefansson, Sigurd O.; Helvik, Jon Vidar

doi:10.1002/cne.23125

Cited by 33 publications

(55 citation statements)

References 72 publications

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“…Consequently, we restricted additional analysis to opn4m . These data were in agreement with previous studies in chicken [24], although differences have been observed in salmon [48] and developing chicks [45]. …”

Section: Resultssupporting

confidence: 94%

“…Whereas the IF circuit was distributed throughout the entire eye, we found that melanopsin-positive mRGCs and mHCs were distributed preferentially in the peripheral retina. mHCs are present in lower vertebrates [21,22,44,45,48,50,61], but are probably absent from mammals. The role of mHCs in lower vertebrates is not completely understood, although the data suggest a role in sensing ambient light [50,61].…”

Section: Discussionmentioning

confidence: 99%

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Wiring the retinal circuits activated by light during early development

2014

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BackgroundLight information is sorted by neuronal circuits to generate image-forming (IF) (interpretation and tracking of visual objects and patterns) and non-image-forming (NIF) tasks. Among the NIF tasks, photic entrainment of circadian rhythms, the pupillary light reflex, and sleep are all associated with physiological responses, mediated mainly by a small group of melanopsin-expressing retinal ganglion cells (mRGCs). Using Xenopus laevis as a model system, and analyzing the c-fos expression induced by light as a surrogate marker of neural activity, we aimed to establish the developmental time at which the cells participating in both systems come on-line in the retina.ResultsWe found that the peripheral retina contains 80% of the two melanopsin-expressing cell types we identified in Xenopus: melanopsin-expressing horizontal cells (mHCs; opn4m+/opn4x+/Prox1+) and mRGCs (2.7% of the total RGCs; opn4m+/opn4x+/Pax6+/Isl1), in a ratio of 6:1. Only mRGCs induced c-fos expression in response to light. Dopaminergic (tyrosine hydroxylase-positive; TH+) amacrine cells (ACs) may be part of the melanopsin-mediated circuit, as shown by preferential c-fos induction by blue light. In the central retina, two cell types in the inner nuclear layer (INL) showed light-mediated induction of c-fos expression [(On-bipolar cells (Otx2+/Isl1+), and a sub-population of ACs (Pax6−/Isl1−)], as well as two RGC sub-populations (Isl1+/Pax6+ and Isl1+/Pax6−). Melanopsin and opsin expression turned on a day before the point at which c-fos expression could first be activated by light (Stage 37/38), in cells of both the classic vision circuit, and those that participate in the retinal component of the NIF circuit. Key to the classic vision circuit is that the component cells engage from the beginning as functional ‘unit circuits’ of two to three cells in the INL for every RGC, with subsequent growth of the vision circuit occurring by the wiring in of more units.ConclusionsWe identified melanopsin-expressing cells and specific cell types in the INL and the RGC layer which induce c-fos expression in response to light, and we determined the developmental time when they become active. We suggest an initial formulation of retinal circuits corresponding to the classic vision pathway and melanopsin-mediated circuits to which they may contribute.

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Section: Resultssupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Wiring the retinal circuits activated by light during early development

2014

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“…5 A , C , and E ). In studies addressing specific sets of duplicate genes (e.g., Macqueen et al 2010, 2013; Rønnestad et al 2010; Sandbakken et al 2012), the percent ID between paralogs ranges from less than 70% to over 85%. Similarly, when we looked at synonymous substitution rates, less divergence was observed within pairs on different chromosomes (mean Ks = 0.40, median Ks = 0.27) compared with pairs derived from the same chromosome (mean Ks = 0.23, median Ks = 0.21) ( t 41.4 = 2.46, P = 0.018).…”

Section: Resultsmentioning

confidence: 99%

“…Genome-wide approaches such as ours will be complemented by studying specific gene families , as has been done in leptins (Rønnestad et al 2010), akirins (Macqueen et al 2010), insulin-like growth factor binding proteins (Macqueen et al 2013), and melanopsins (Sandbakken et al 2012). Such approaches can look at the fine details of gene duplication in individual case, which is beyond the scope of our genome-wide approach.…”

Section: Discussionmentioning

confidence: 99%

Extensive Local Gene Duplication and Functional Divergence among Paralogs in Atlantic Salmon

Warren¹,

Ciborowski²,

Casadei³

et al. 2014

Genome Biology and Evolution

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Many organisms can generate alternative phenotypes from the same genome, enabling individuals to exploit diverse and variable environments. A prevailing hypothesis is that such adaptation has been favored by gene duplication events, which generate redundant genomic material that may evolve divergent functions. Vertebrate examples of recent whole-genome duplications are sparse although one example is the salmonids, which have undergone a whole-genome duplication event within the last 100 Myr. The life-cycle of the Atlantic salmon, Salmo salar, depends on the ability to produce alternating phenotypes from the same genome, to facilitate migration and maintain its anadromous life history. Here, we investigate the hypothesis that genome-wide and local gene duplication events have contributed to the salmonid adaptation. We used high-throughput sequencing to characterize the transcriptomes of three key organs involved in regulating migration in S. salar: Brain, pituitary, and olfactory epithelium. We identified over 10,000 undescribed S. salar sequences and designed an analytic workflow to distinguish between paralogs originating from local gene duplication events or from whole-genome duplication events. These data reveal that substantial local gene duplications took place shortly after the whole-genome duplication event. Many of the identified paralog pairs have either diverged in function or become noncoding. Future functional genomics studies will reveal to what extent this rich source of divergence in genetic sequence is likely to have facilitated the evolution of extreme phenotypic plasticity required for an anadromous life-cycle.

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“…A polyclonal antibody against serotonin (20080; Immunostar, Hudson, WI; RRID:AB_10718516) raised in rabbit was used to detect serotonin. According to the manufacturer, this antibody is specific toward its target in a variety of vertebrate species and has been used in studies of the Atlantic salmon, Salmon salar , (Sandbakken, Ebbesson, Stefansson, & Helvik, ), and sea lamprey (Villar‐Cerviño et al, ). Additionally, the manufacturer states that the antibody serum does not react with 5‐hydroxytryptophan, 5‐hydroxyinodole‐3‐acetic acid and dopamine in cross‐reactivity experiments.…”

Section: Methodsmentioning

confidence: 99%

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

Rosner

Rohmann

Bass

et al. 2018

J of Comparative Neurology

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Vocalization is a behavioral feature that is shared among multiple vertebrate lineages, including fish. The temporal patterning of vocal communication signals is set, in part, by central pattern generators (CPGs). Toadfishes are well‐established models for CPG coding of vocalization at the hindbrain level. The vocal CPG comprises three topographically separate nuclei: pre‐pacemaker, pacemaker, motor. While the connectivity between these nuclei is well understood, their neurochemical profile remains largely unexplored. The highly vocal Gulf toadfish, Opsanus beta, has been the subject of previous behavioral, neuroanatomical and neurophysiological studies. Combining transneuronal neurobiotin‐labeling with immunohistochemistry, we map the distribution of inhibitory neurotransmitters and neuromodulators along with gap junctions in the vocal CPG of this species. Dense GABAergic and glycinergic label is found throughout the CPG, with labeled somata immediately adjacent to or within CPG nuclei, including a distinct subset of pacemaker neurons co‐labeled with neurobiotin and glycine. Neurobiotin‐labeled motor and pacemaker neurons are densely co‐labeled with the gap junction protein connexin 35/36, supporting the hypothesis that transneuronal neurobiotin‐labeling occurs, at least in part, via gap junction coupling. Serotonergic and catecholaminergic label is also robust within the entire vocal CPG, with additional cholinergic label in pacemaker and prepacemaker nuclei. Likely sources of these putative modulatory inputs are neurons within or immediately adjacent to vocal CPG neurons. Together with prior neurophysiological investigations, the results reveal potential mechanisms for generating multiple classes of social context‐dependent vocalizations with widely divergent temporal and spectral properties.

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Isolation and characterization of melanopsin photoreceptors of atlantic salmon (Salmo salar)

Cited by 33 publications

References 72 publications

Wiring the retinal circuits activated by light during early development

Wiring the retinal circuits activated by light during early development

Extensive Local Gene Duplication and Functional Divergence among Paralogs in Atlantic Salmon

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

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