Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

AbstractCiliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor evolution in animals. The two photoreceptor-cell types coexist in some animals, however how they functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming to non-directional UV light, a behavior absent in ciliary-opsin knockouts. UV avoidance antagonizes positive phototaxis mediated by the rhabdomeric eyes so that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during planktonic migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptors with implications for eye and photoreceptor evolution.

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Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

eLife ◽

10.7554/elife.36440 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 11

Author(s):

Csaba Verasztó ◽

Martin Gühmann ◽

Huiyong Jia ◽

Vinoth Babu Veedin Rajan ◽

Luis A Bezares-Calderón ◽

...

Keyword(s):

Photoreceptor Cell ◽

Uv Light ◽

Functional Integration ◽

Photoreceptor Cells ◽

Cell Types ◽

Planktonic Larva ◽

Marine Zooplankton ◽

Rhabdomeric Photoreceptor ◽

Depth Gauge ◽

Rhabdomeric Photoreceptor Cells

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor-cell evolution in animals. The two cell types coexist in some animals, however how these cells functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming in non-directional UV light, a behavior absent in ciliary-opsin knockout larvae. UV avoidance overrides positive phototaxis mediated by the rhabdomeric eyes such that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during vertical migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptor cells in a zooplankton larva.

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Reconstructing the eyes of Urbilateria

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2001.0971 ◽

2001 ◽

Vol 356 (1414) ◽

pp. 1545-1563 ◽

Cited By ~ 120

Author(s):

Detlev Arendt ◽

Joachim Wittbrodt

Keyword(s):

Photoreceptor Cell ◽

Molecular Level ◽

Pigment Cell ◽

Photoreceptor Cells ◽

Cell Types ◽

Rhabdomeric Photoreceptor ◽

Left And Right ◽

The Common ◽

Shared Roles ◽

Rhabdomeric Photoreceptor Cells

The shared roles of Pax6 and Six homologues in the eye development of various bilaterians suggest that Urbilateria, the common ancestors of all Bilateria, already possessed some simple form of eyes. Here, we re–address the homology of bilaterian cerebral eyes at the level of eye anatomy, of eye–constituting cell types and of phototransductory molecules. The most widespread eye type found in Bilateria are the larval pigment–cup eyes located to the left and right of the apical organ in primary, ciliary larvae of Protostomia and Deuterostomia. They can be as simple as comprising a single pigment cell and a single photoreceptor cell in inverse orientation. Another more elaborate type of cerebral pigment–cup eyes with an everse arrangement of photoreceptor cells is found in adult Protostomia. Both inverse larval and everse adult eyes employ rhabdomeric photoreceptor cells and thus differ from the chordate cerebral eyes with ciliary photoreceptors. This is highly significant because on the molecular level we find that for phototransduction rhabdomeric versus ciliary photoreceptor cells employ divergent rhodopsins and non–orthologous G–proteins, rhodopsin kinases and arrestins. Our comparison supports homology of cerebral eyes in Protostomia; it challenges, however, homology of chordate and non–chordate cerebral eyes that employ photoreceptor cells with non–orthologous phototransductory cascades.

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Author response: Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

10.7554/elife.36440.024 ◽

2018 ◽

Cited By ~ 2

Author(s):

Csaba Verasztó ◽

Martin Gühmann ◽

Huiyong Jia ◽

Vinoth Babu Veedin Rajan ◽

Luis A Bezares-Calderón ◽

...

Keyword(s):

Photoreceptor Cell ◽

Author Response ◽

Marine Zooplankton ◽

Rhabdomeric Photoreceptor ◽

Depth Gauge

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Decision letter: Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

10.7554/elife.36440.023 ◽

2018 ◽

Keyword(s):

Photoreceptor Cell ◽

Marine Zooplankton ◽

Rhabdomeric Photoreceptor ◽

Depth Gauge

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Cytoplasmic Characteristics of Three Different Rhabdomeric Photoreceptor Cells in a Marine Gastropod, Onchidium verruculatum

Journal of Electron Microscopy ◽

10.1093/oxfordjournals.jmicro.a050448 ◽

1984 ◽

Keyword(s):

Photoreceptor Cells ◽

Marine Gastropod ◽

Rhabdomeric Photoreceptor ◽

Rhabdomeric Photoreceptor Cells

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Evolution of clitellate phaosomes from rhabdomeric photoreceptor cells of polychaetes – a study in the leech Helobdella robusta (Annelida, Sedentaria, Clitellata)

Frontiers in Zoology ◽

10.1186/1742-9994-10-52 ◽

2013 ◽

Vol 10 (1) ◽

pp. 52 ◽

Cited By ~ 7

Author(s):

Carmen Döring ◽

Jasmin Gosda ◽

Kristin Tessmar-Raible ◽

Harald Hausen ◽

Detlev Arendt ◽

...

Keyword(s):

Photoreceptor Cells ◽

Helobdella Robusta ◽

Rhabdomeric Photoreceptor ◽

Rhabdomeric Photoreceptor Cells

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Understanding the dermal light sense in the context of integrative photoreceptor cell biology

Visual Neuroscience ◽

10.1017/s0952523811000150 ◽

2011 ◽

Vol 28 (4) ◽

pp. 265-279 ◽

Cited By ~ 38

Author(s):

M. DESMOND RAMIREZ ◽

DANIEL I. SPEISER ◽

M. SABRINA PANKEY ◽

TODD H. OAKLEY

Keyword(s):

Photoreceptor Cell ◽

Classification Scheme ◽

Photoreceptor Cells ◽

Cell Types ◽

High Order ◽

Molecular Techniques ◽

Physiological Data ◽

New Classification ◽

Directional Information ◽

First Order

AbstractWhile the concept of a dermal light sense has existed for over a century, little progress has been made in our understanding of the mechanisms underlying dispersed photoreception and the evolutionary histories of dispersed photoreceptor cells. These cells historically have been difficult to locate and positively identify, but modern molecular techniques, integrated with existing behavioral, morphological, and physiological data, will make cell identification easier and allow us to address questions of mechanism and evolution. With this in mind, we propose a new classification scheme for all photoreceptor cell types based on two axes, cell distribution (aggregated vs. dispersed) and position within neural networks (first order vs. high order). All photoreceptor cells fall within one of four quadrants created by these axes: aggregated/high order, dispersed/high order, aggregated/first order, or dispersed/first order. This new method of organization will help researchers make objective comparisons between different photoreceptor cell types. Using integrative data from four major phyla (Mollusca, Cnidaria, Echinodermata, and Arthropoda), we also provide evidence for three hypotheses for dispersed photoreceptor cell function and evolution. First, aside from echinoderms, we find that animals often use dispersed photoreceptor cells for tasks that do not require spatial vision. Second, although there are both echinoderm and arthropod exceptions, we find that dispersed photoreceptor cells generally lack morphological specializations that either enhance light gathering or aid in the collection of directional information about light. Third, we find that dispersed photoreceptor cells have evolved a number of times in Metazoa and that most dispersed photoreceptor cells have likely evolved through the co-option of existing phototransduction cascades. Our new classification scheme, combined with modern investigative techniques, will help us address these hypotheses in great detail and generate new hypothesis regarding the function and evolution of dispersed photoreceptor cells.

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Distinct and Atypical Intrinsic and Extrinsic Cell Death Pathways between Photoreceptor Cell Types upon Specific Ablation of Ranbp2 in Cone Photoreceptors

PLoS Genetics ◽

10.1371/journal.pgen.1003555 ◽

2013 ◽

Vol 9 (6) ◽

pp. e1003555 ◽

Cited By ~ 21

Author(s):

Kyoung-in Cho ◽

MdEmdadul Haque ◽

Jessica Wang ◽

Minzhong Yu ◽

Ying Hao ◽

...

Keyword(s):

Cell Death ◽

Photoreceptor Cell ◽

Cell Types ◽

Cone Photoreceptors ◽

Cell Death Pathways

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Virus-Mediated Transduction of Murine Retina with Adeno-Associated Virus: Effects of Viral Capsid and Genome Size

Journal of Virology ◽

10.1128/jvi.76.15.7651-7660.2002 ◽

2002 ◽

Vol 76 (15) ◽

pp. 7651-7660 ◽

Cited By ~ 126

Author(s):

Grace S. Yang ◽

Michael Schmidt ◽

Ziying Yan ◽

Jonathan D. Lindbloom ◽

Thomas C. Harding ◽

...

Keyword(s):

Gene Transfer ◽

Photoreceptor Cells ◽

Cell Types ◽

Full Length ◽

Specific Cell ◽

Adeno Associated Virus ◽

Gene Therapy Vectors ◽

Retinal Degenerative Diseases ◽

Or Gene ◽

Half Length

ABSTRACT Gene therapy vectors based on adeno-associated viruses (AAVs) show promise for the treatment of retinal degenerative diseases. In prior work, subretinal injections of AAV2, AAV5, and AAV2 pseudotyped with AAV5 capsids (AAV2/5) showed variable retinal pigmented epithelium (RPE) and photoreceptor cell transduction, while AAV2/1 predominantly transduced the RPE. To more thoroughly compare the efficiencies of gene transfer of AAV2, AAV3, AAV5, and AAV6, we quantified, using stereological methods, the kinetics and efficiency of AAV transduction to mouse photoreceptor cells. We observed persistent photoreceptor and RPE transduction by AAV5 and AAV2 up to 31 weeks and found that AAV5 transduced a greater volume than AAV2. AAV5 containing full-length or half-length genomes and AAV2/5 transduced comparable numbers of photoreceptor cells with similar rates of onset of expression. Compared to AAV2, AAV5 transduced significantly greater numbers of photoreceptor cells at 5 and 15 weeks after surgery (greater than 1,000 times and up to 400 times more, respectively). Also, there were 30 times more genome copies in eyes injected with AAV2/5 than in eyes injected with AAV2. Comparing AAVs with half-length genomes, AAV5 transduced only four times more photoreceptor cells than AAV2 at 5 weeks and nearly equivalent numbers at 15 weeks. The enhancement of transduction was seen at the DNA level, with 50 times more viral genome copies in retinas injected with AAV having short genomes than in retinas injected with AAV containing full-length ones. Subretinal injection of AAV2/6 showed only RPE transduction at 5 and 15 weeks, while AAV2/3 did not transduce retinal cells. We conclude that varying genome length and AAV capsids may allow for improved expression and/or gene transfer to specific cell types in the retina.

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