An Unexpected Diversity of Photoreceptor Classes in the Longfin Squid, Doryteuthis pealeii

Kingston, Alexandra C. N.; Wardill, Trevor J.; Hanlon, Roger T.; Cronin, Thomas W.

doi:10.1371/journal.pone.0135381

Cited by 23 publications

(30 citation statements)

References 25 publications

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“…Right: Morphological key for the cephalopod eye, showing the rhabdoms (r), proximal region/supporting cell layer (p/s), inner segments (is), photoreceptor nuclei (n), and plexiform layer (pl). For comparative labeling in the eye, es-rhodopsin expression occurred at the extreme ends of the rhabdoms similar to the protein localization in another squid species ( Doryteuthis pealeii ; Kingston et al 2015), but also extended into the inner segments. Labeling of es-crumbs occurred within the inner segments.…”

Section: Figurementioning

confidence: 73%

“…As a complementary experiment, we examined histological samples of the light organ and eye using paraffin-section ISH methods as previously described (Peyer et al 2014). In the eye, we localized es-crumbs along with es-rhodopsin to confirm that both genes occur in regions of the photoreceptors similar to other animals (Kingston et al 2015; Hsu and Jensen 2010). We included rhodopsin because it is a common reference gene in the eye.…”

Section: Methodsmentioning

confidence: 80%

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Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid–vibrio light organ symbiosis

Peyer¹,

Heath‐Heckman

McFall‐Ngai

2017

Dev Genes Evol

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The protein Crumbs is a determinant of apical-basal cell polarity and plays a role in apoptosis of epithelial cells and their protection against photodamage. Using the squid-vibrio system, a model for development of symbiotic partnerships, we examined the modulation of the crumbs gene in host epithelial tissues during initiation and maintenance of the association. The extracellular luminous symbiont Vibrio fischeri colonizes the apical surfaces of polarized epithelia in deep crypts of the Euprymna scolopes light organ. During initial colonization each generation, symbiont harvesting is potentiated by the biochemical and biophysical activity of superficial ciliated epithelia, which are several cell layers from the crypt epithelia where the symbionts reside. Within hours of crypt colonization, the symbionts induce the cell-death mediated regression of the remote superficial ciliated fields. However, the crypt cells directly interacting with the symbiont are protected from death. In the squid host, we characterized the gene and encoded protein during light-organ morphogenesis and in response to symbiosis. Features of the protein sequence and structure, phylogenetic relationships, and localization patterns in the eye supported assignment of the squid protein to the Crumbs family. In situ hybridization revealed that the crumbs transcript shows opposite expression at the onset of symbiosis in the two different regions of the light organ: elevated levels in the superficial epithelia were attenuated whereas low levels in the crypt epithelia were turned up. Although a rhythmic association in which the host controls the symbiont population over the day-night cycle begins in the juvenile upon colonization, cycling of crumbs was evident only in the adult organ with peak expression coincident with maximum symbiont population and luminescence. Our results provide evidence that crumbs responds to symbiont cues that induce developmental apoptosis and to symbiont population dynamics correlating with luminescence-based stress throughout the duration of the host-microbe association.

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Section: Figurementioning

confidence: 73%

Section: Methodsmentioning

confidence: 80%

Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid–vibrio light organ symbiosis

Peyer¹,

Heath‐Heckman

McFall‐Ngai

2017

Dev Genes Evol

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“…Not only are rhodopsin and retinochrome important for the cephalopod visual system, they are also found together in extraocular tissues serving a potential role in camouflage (Kingston et al 2015). By adding a squid retinochrome sequence to our opsin phylogeny we found that the lepidopteran-specific unclassified opsin and RGR-like opsin are more closely-related to retinochrome than they are to other opsins with known functions ( Figure 4A).…”

Section: Opsins In Lepidopteramentioning

confidence: 97%

Evolution of Phototransduction Genes in Lepidoptera

Macias-Muñoz¹,

Briscoe²

2019

Preprint

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Vision is underpinned by phototransduction, a signaling cascade that converts light energy into an electrical signal. Among insects, phototransduction is best understood in Drosophila melanogaster. A survey of phototransduction genes in four insect genomes found gains and losses between D. melanogaster and other insects; this study did not include lepidopterans. Diurnal butterflies and nocturnal moths occupy different light environments and have distinct eye morphologies, which might impact the expression of their phototransduction genes. Here, we used transcriptomics and phylogenetics to identify phototransduction genes that vary between D. melanogaster and Lepidoptera, and between moths and butterflies. Most phototransduction genes were conserved between D. melanogaster and Lepidoptera, with some exceptions. We found two lepidopteran opsins lacking a D. melanogaster ortholog, and using antibodies found that one, a candidate retinochrome which we name unclassified opsin (UnRh), is expressed in the crystaline cone cells and the pigment cells of the butterfly Heliconius melpomene. We also found differences between Lepidoptera and D. melanogaster phototransduction in diacylglycerol regulation where a lepidopteran paralog, DAG, may be taking on a role in vision. Lastly, butterflies express similar amounts of trp and trpl channel mRNAs, while moths express approximately 50x less trp. Since TRP/TRPL channels allow Ca 2+ and Na + influx this might explain why moths appear to express less Calx and Nckx30C Na + /Ca 2+ channel mRNAs. Our findings suggest that while many single-copy D. melanogaster phototransduction genes are conserved in lepidopterans, phototransduction gene expression differences exist between moths and butterflies that may be linked to their visual light environment. 4 downstream pathway by which opsins function might also contribute to differences in visual systems (Plachetzki et al. 2010). Fewer studies have investigated the downstream phototransduction cascade in non-D. melanogaster insects. Studies of phototransduction in other insects have focused on presence, absence, or relative expression of genes in head transcriptomes. In the troglobiont beetle, Ptomaphagus hirtus, for example, 20 genes were identified from adult head mRNA (Friedrich et al. 2011). Exposure of the oriental armyworm, Mythimna separate, to different light environments resulted in differential expression of phototransduction genes in adult heads (Duan et al. 2017). Similarly, phototransduction genes were also differentially expressed between seasonal forms in heads of the butterfly Bicyclus anynana (Macias-Muñoz et al. 2016). One study quantified opsin and TRP channel gene expression and used RNAi to determine that opsin has the largest effect on phototransduction in the nocturnal cockroach Periplaneta americana (but see below)(French et al. 2015). Yet, it remains largely unknown how variable the phototransduction cascade is between insect species.Lepidoptera, moths and butterflies, provide an interesting group in which to invest...

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“…The recently published octopus genome (22) did not identify any additional opsins using both whole-genome sequencing and transcriptome sequencing of skin tissue, despite a focus on identifying G protein-coupled receptors. Across a diversity of taxa, all cephalopod studies to date have found rhodopsin transcripts in the skin identical to those in the eye (23), and the skin's spectral response to light is nearly identical to that of the retina (24). Given multiple strong lines of evidence against additional undiscovered skin opsins and no described mechanism for spectral discrimination arising from rhodopsin alone, this competing hypothesis is not currently viable.…”

Section: Contradictory Evidence: Chromatic Behavior But a Single Opsinmentioning

confidence: 99%

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

Stubbs

2016

Proc. Natl. Acad. Sci. U.S.A.

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We present a mechanism by which organisms with only a single photoreceptor, which have a monochromatic view of the world, can achieve color discrimination. An off-axis pupil and the principle of chromatic aberration (where different wavelengths come to focus at different distances behind a lens) can combine to provide "colorblind" animals with a way to distinguish colors. As a specific example, we constructed a computer model of the visual system of cephalopods (octopus, squid, and cuttlefish) that have a single unfiltered photoreceptor type. We compute a quantitative image quality budget for this visual system and show how chromatic blurring dominates the visual acuity in these animals in shallow water. We quantitatively show, through numerical simulations, how chromatic aberration can be exploited to obtain spectral information, especially through nonaxial pupils that are characteristic of coleoid cephalopods. We have also assessed the inherent ambiguity between range and color that is a consequence of the chromatic variation of best focus with wavelength. This proposed mechanism is consistent with the extensive suite of visual/behavioral and physiological data that has been obtained from cephalopod studies and offers a possible solution to the apparent paradox of vivid chromatic behaviors in color blind animals. Moreover, this proposed mechanism has potential applicability in organisms with limited photoreceptor complements, such as spiders and dolphins.spectral discrimination | chromatic aberration | color vision | pupil shape | cephalopod W e show in this paper that, under certain conditions, organisms can determine the spectral composition of objects, even with a single photoreceptor type. Through computational modeling, we show a mechanism that provides spectral information using an important relationship: the position of sharpest focus depends on the spectral peak of detected photons. Mapping out contrast vs. focal setting (accommodation) amounts to obtaining a coarse spectrum of objects in the field of view, much as a digital camera attains best focus by maximizing contrast vs. focal length. We note that a similar phenomenon has been advanced as a possible explanation for color percepts in red/green color-blind primates (1); however, primates have not evolved the off-axis pupil shape found in nearly all shallow water cephalopods that enhances this effect.The only other known mechanism of color discrimination in organisms involves determining the spectrum of electromagnetic radiation using differential comparisons between simultaneous neural signals arising from photoreceptor channels with differing spectral acceptances. Color vision using multiple classes of photoreceptors on a 2D retinal surface comes at a cost: reduced signal to noise ratio in low-light conditions and degraded angular resolution in each spectral channel. Thus, many lineages that are or were active in low-light conditions have lost spectral channels to increase sensitivity (2).Octopus, squid, and cuttlefish (coleoid cephalopods) have l...

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An Unexpected Diversity of Photoreceptor Classes in the Longfin Squid, Doryteuthis pealeii

Cited by 23 publications

References 25 publications

Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid–vibrio light organ symbiosis

Characterization of the cell polarity gene crumbs during the early development and maintenance of the squid–vibrio light organ symbiosis

Evolution of Phototransduction Genes in Lepidoptera

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

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