Amphioxus photoreceptors - insights into the evolution of vertebrate opsins, vision and circadian rhythmicity

Abstract

Studies on amphioxus, representing the most basal group of chordates, can give insights 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 hypotheses about the history of these features during chordate and subsequently vertebrate evolution.

Cellular and molecular mechanisms of photoreceptor tuning for prey capture in larval zebrafish

“…Building on our exquisite understanding on phototransduction in general (Fain et al, 2010;Lamb, 2013;Pergner and Kozmik, 2017;Pugh and Lamb, 1993;Yau and Hardie, 2009), each of these regulatory changes can be quantitatively linked to a specific functional effect (Invergo et al, 2013(Invergo et al, , 2014. In particular, the tonic level of outer segment cGMP is key as it determines the open-probability of cyclicnucleotide gated (CNG) channels which define the cone's dark current to ultimately set the calcium baseline in the cone pedicle through the opening or closing of synaptic voltage gated calcium channels (Fain et al, 2010;Lamb, 2013;Pergner and Kozmik, 2017). Here, upregulation of guanylate cyclase 3 (Dizhoor and Hurley, 1999;Hurley, 1987;Kuhn, 2016) (gc3) is expected to boost the rate of cyclic guanosine monophosphate (cGMP) synthesis from guanosine triphosphate (GTP) to open CNG channels, depolarising the cone and thus rising synaptic calcium baseline.…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…The simple light‐detecting circuit of the lamprey larva may have an evolutionary affinity to that of amphioxus. Amphioxus has four types of photoreceptors: the frontal eye, Hesse ocelli, Joseph cells and lamellar body (Lacalli, ; Pergner & Kozmik, ). Among them, the frontal eye is central because it is homologous to the vertebrate retina.…”

Parallel Visual Circuitry in a Basal Chordate

“…Amphioxus by contrast, has four distinct photoreceptive organs [53]. The amphioxus frontal eye has been proposed as homologous to the vertebrate lateral eyes, while the lamellar body is thought to be homologous to the vertebrate pineal organ [53,54]. The other two amphioxus photoreceptor types, the dorsal ocelli and the Joseph cells, are thought, based on a number of criteria, including their rhabdomeric morphology-which differs from the ciliary morphology of vertebrate and ascidian photoreceptors-to be vestiges of a more primitive photoreceptive system.…”

“…Vertebrates are characterized by the presence of both paired lateral (i.e., retinal) eyes, and an unpaired medial/pineal eye [52]. Amphioxus by contrast, has four distinct photoreceptive organs [53]. The amphioxus frontal eye has been proposed as homologous to the vertebrate lateral eyes, while the lamellar body is thought to be homologous to the vertebrate pineal organ [53,54].…”