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Cells
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Eye Development and Evolution: Cellular and Molecular Events
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Eye Development and Evolution: Cellular and Molecular Events

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Tissues and Organs".

Deadline for manuscript submissions: closed (31 July 2024) | Viewed by 19858

Special Issue Editors

Dr. Annamaria Locascio

E-Mail Website
Guest Editor
Department of Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn, Naples, Italy
Interests: molecular and cellular basis of evolution and development; developmental gene regulatory networks; vertebrate evolution; eye evolution; eye development; molecular evolutionary genetics; marine biology
Dr. Maria I. Arnone

E-Mail Website
Guest Editor
Department of Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn, Naples, Italy
Interests: evolution of organs and body parts; Gene Regulatory Networks (GRN); Strongylocentrotus purpuratus model system biology

Special Issue Information

Dear Colleagues,

Although significant progress has been made in recent decades in deciphering the cascade of events responsible for eye formation and evolution, these complex processes are far from being clearly delineated. Comparative molecular approaches dissecting developmental mechanisms in different visual systems have played an essential role in elucidating the evolutionary steps through which a light-sensitive pigmented cell on the skin has gone through changes and complexities during the evolution of cones, rods, and the vertebrate retina. More recently, dissecting the developmental programs at single-cell resolution and providing a panel of molecular tools to shed light on the formation of the different eye structures in metazoans have been of primary interest for the scientific community in the field.

This Special Issue aims to summarize current knowledge and to add breakthrough findings that could improve our understanding of the different and progressively more complex visual structures that accompanied metazoan evolution. We are looking for original research and review articles that will contribute to deciphering the molecular and cellular events involved in early eye specification in the anterior brain, its differentiation in functional domains, and its structural organization in different animals. This Special Issue will focus on deep developmental and comparative-evolutionary analysis, and will provide new important information on the molecular and cellular mechanisms responsible for the formation and functioning of complex eye structures. A deeper understanding of the basic and essential mechanisms at the base of the formation and the evolution of different animal eyes may ultimately help to shed light on the emergence of human eye genetic disorders.

We are looking forward to your contributions to this Special Issue.

Dr. Annamaria Locascio
Dr. Maria I. Arnone
Guest Editors

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Light-sensitive pigmented cells
  • Evolution of pigmented cells
  • Retina cells
  • Eye development
  • Eye evolution
  • Eye specification
  • Eye differentiation
  • Comparative-evolutionary analysis
  • Molecular and cellular mechanisms of eye formation and evolution.

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Published Papers (6 papers)

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Research

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17 pages, 2945 KiB  
Article
Single-Cell Transcriptomic Analysis Reveals the Molecular Profile of Go-Opsin Photoreceptor Cells in Sea Urchin Larvae
by Maria Cocurullo, Periklis Paganos, Rossella Annunziata, Danila Voronov and Maria Ina Arnone
Cells 2023, 12(17), 2134; https://doi.org/10.3390/cells12172134 - 23 Aug 2023
Cited by 3 | Viewed by 1768
Abstract
The ability to perceive and respond to light stimuli is fundamental not only for spatial vision but also to many other light-mediated interactions with the environment. In animals, light perception is performed by specific cells known as photoreceptors and, at molecular level, by [...] Read more.
The ability to perceive and respond to light stimuli is fundamental not only for spatial vision but also to many other light-mediated interactions with the environment. In animals, light perception is performed by specific cells known as photoreceptors and, at molecular level, by a group of GPCRs known as opsins. Sea urchin larvae possess a group of photoreceptor cells (PRCs) deploying a Go-Opsin (Opsin3.2) which have been shown to share transcription factors and morphology with PRCs of the ciliary type, raising new questions related to how this sea urchin larva PRC is specified and whether it shares a common ancestor with ciliary PRCs or it if evolved independently through convergent evolution. To answer these questions, we combined immunohistochemistry and fluorescent in situ hybridization to investigate how the Opsin3.2 PRCs develop in the sea urchin Strongylocentrotus purpuratus larva. Subsequently, we applied single-cell transcriptomics to investigate the molecular signature of the Sp-Opsin3.2-expressing cells and show that they deploy an ancient regulatory program responsible for photoreceptors specification. Finally, we also discuss the possible functions of the Opsin3.2-positive cells based on their molecular fingerprint, and we suggest that they are involved in a variety of signaling pathways, including those entailing the thyrotropin-releasing hormone. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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21 pages, 6382 KiB  
Article
A New Model Organism to Investigate Extraocular Photoreception: Opsin and Retinal Gene Expression in the Sea Urchin Paracentrotus lividus
by Periklis Paganos, Esther Ullrich-Lüter, Filomena Caccavale, Anne Zakrzewski, Danila Voronov, Inés Fournon-Berodia, Maria Cocurullo, Carsten Lüter and Maria Ina Arnone
Cells 2022, 11(17), 2636; https://doi.org/10.3390/cells11172636 - 24 Aug 2022
Cited by 8 | Viewed by 3101
Abstract
Molecular research on the evolution of extraocular photoreception has drawn attention to photosensitive animals lacking proper eye organs. Outside of vertebrates, little is known about this type of sensory system in any other deuterostome. In this study, we investigate such an extraocular photoreceptor [...] Read more.
Molecular research on the evolution of extraocular photoreception has drawn attention to photosensitive animals lacking proper eye organs. Outside of vertebrates, little is known about this type of sensory system in any other deuterostome. In this study, we investigate such an extraocular photoreceptor cell (PRC) system in developmental stages of the sea urchin Paracentrotus lividus. We provide a general overview of the cell type families present at the mature rudiment stage using single-cell transcriptomics, while emphasizing the PRCs complexity. We show that three neuronal and one muscle-like PRC type families express retinal genes prior to metamorphosis. Two of the three neuronal PRC type families express a rhabdomeric opsin as well as an echinoderm-specific opsin (echinopsin), and their genetic wiring includes sea urchin orthologs of key retinal genes such as hlf, pp2ab56e, barh, otx, ac/sc, brn3, six1/2, pax6, six3, neuroD, irxA, isl and ato. Using qPCR, in situ hybridization, and immunohistochemical analysis, we found that the expressed retinal gene composition becomes more complex from mature rudiment to juvenile stage. The majority of retinal genes are expressed dominantly in the animals’ podia, and in addition to the genes already expressed in the mature rudiment, the juvenile podia express a ciliary opsin, another echinopsin, and two Go-opsins. The expression of a core of vertebrate retinal gene orthologs indicates that sea urchins have an evolutionarily conserved gene regulatory toolkit that controls photoreceptor specification and function, and that their podia are photosensory organs. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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21 pages, 1473 KiB  
Article
The Gluopsins: Opsins without the Retinal Binding Lysine
by Martin Gühmann, Megan L. Porter and Michael J. Bok
Cells 2022, 11(15), 2441; https://doi.org/10.3390/cells11152441 - 6 Aug 2022
Cited by 9 | Viewed by 4122
Abstract
Opsins allow us to see. They are G-protein-coupled receptors and bind as ligand retinal, which is bound covalently to a lysine in the seventh transmembrane domain. This makes opsins light-sensitive. The lysine is so conserved that it is used to define a sequence [...] Read more.
Opsins allow us to see. They are G-protein-coupled receptors and bind as ligand retinal, which is bound covalently to a lysine in the seventh transmembrane domain. This makes opsins light-sensitive. The lysine is so conserved that it is used to define a sequence as an opsin and thus phylogenetic opsin reconstructions discard any sequence without it. However, recently, opsins were found that function not only as photoreceptors but also as chemoreceptors. For chemoreception, the lysine is not needed. Therefore, we wondered: Do opsins exists that have lost this lysine during evolution? To find such opsins, we built an automatic pipeline for reconstructing a large-scale opsin phylogeny. The pipeline compiles and aligns sequences from public sources, reconstructs the phylogeny, prunes rogue sequences, and visualizes the resulting tree. Our final opsin phylogeny is the largest to date with 4956 opsins. Among them is a clade of 33 opsins that have the lysine replaced by glutamic acid. Thus, we call them gluopsins. The gluopsins are mainly dragonfly and butterfly opsins, closely related to the RGR-opsins and the retinochromes. Like those, they have a derived NPxxY motif. However, what their particular function is, remains to be seen. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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18 pages, 3683 KiB  
Article
Regulation of Eye Determination and Regionalization in the Spider Parasteatoda tepidariorum
by Luis Baudouin-Gonzalez, Amber Harper, Alistair P. McGregor and Lauren Sumner-Rooney
Cells 2022, 11(4), 631; https://doi.org/10.3390/cells11040631 - 11 Feb 2022
Cited by 6 | Viewed by 5161
Abstract
Animal visual systems are enormously diverse, but their development appears to be controlled by a set of conserved retinal determination genes (RDGs). Spiders are particular masters of visual system innovation, and offer an excellent opportunity to study the evolution of animal eyes. Several [...] Read more.
Animal visual systems are enormously diverse, but their development appears to be controlled by a set of conserved retinal determination genes (RDGs). Spiders are particular masters of visual system innovation, and offer an excellent opportunity to study the evolution of animal eyes. Several RDGs have been identified in spider eye primordia, but their interactions and regulation remain unclear. From our knowledge of RDG network regulation in Drosophila melanogaster, we hypothesize that orthologs of Pax6, eyegone, Wnt genes, hh, dpp, and atonal could play important roles in controlling eye development in spiders. We analyzed the expression of these genes in developing embryos of the spider Parasteatodatepidariorum, both independently and in relation to the eye primordia, marked using probes for the RDG sine oculis. Our results support conserved roles for Wnt genes in restricting the size and position of the eye field, as well as for atonal initiating photoreceptor differentiation. However, we found no strong evidence for an upstream role of Pax6 in eye development, despite its label as a master regulator of animal eye development; nor do eyg, hh or dpp compensate for the absence of Pax6. Conversely, our results indicate that hh may work with Wnt signaling to restrict eye growth, a role similar to that of Sonichedgehog (Shh) in vertebrates. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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Review

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17 pages, 2746 KiB  
Review
The Formation and Renewal of Photoreceptor Outer Segments
by Jingjin Xu, Chengtian Zhao and Yunsi Kang
Cells 2024, 13(16), 1357; https://doi.org/10.3390/cells13161357 - 15 Aug 2024
Viewed by 1485
Abstract
The visual system is essential for humans to perceive the environment. In the retina, rod and cone photoreceptor neurons are the initial sites where vision forms. The apical region of both cone and rod photoreceptors contains a light-sensing organelle known as the outer [...] Read more.
The visual system is essential for humans to perceive the environment. In the retina, rod and cone photoreceptor neurons are the initial sites where vision forms. The apical region of both cone and rod photoreceptors contains a light-sensing organelle known as the outer segment (OS), which houses tens of thousands of light-sensitive opsins. The OSs of photoreceptors are not static; they require rhythmic renewal to maintain normal physiological functions. Disruptions in OS renewal can lead to various genetic disorders, such as retinitis pigmentosa (RP). Understanding the patterns and molecular mechanisms of photoreceptor OS renewal remains one of the most intriguing topics in visual biology. This review aims to elucidate the structure of photoreceptor OSs, the molecular mechanisms underlying photoreceptor OS renewal, and the retinal diseases resulting from defects in this renewal process. Additionally, we will explore retinal diseases related to photoreceptor OS renewal and potential therapeutic strategies, concluding with a discussion on future research directions for OS renewal. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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23 pages, 2209 KiB  
Review
Deep Diversity: Extensive Variation in the Components of Complex Visual Systems across Animals
by Oliver Vöcking, Aide Macias-Muñoz, Stuart J. Jaeger and Todd H. Oakley
Cells 2022, 11(24), 3966; https://doi.org/10.3390/cells11243966 - 8 Dec 2022
Cited by 7 | Viewed by 2510
Abstract
Understanding the molecular underpinnings of the evolution of complex (multi-part) systems is a fundamental topic in biology. One unanswered question is to what the extent do similar or different genes and regulatory interactions underlie similar complex systems across species? Animal eyes and phototransduction [...] Read more.
Understanding the molecular underpinnings of the evolution of complex (multi-part) systems is a fundamental topic in biology. One unanswered question is to what the extent do similar or different genes and regulatory interactions underlie similar complex systems across species? Animal eyes and phototransduction (light detection) are outstanding systems to investigate this question because some of the genetics underlying these traits are well characterized in model organisms. However, comparative studies using non-model organisms are also necessary to understand the diversity and evolution of these traits. Here, we compare the characteristics of photoreceptor cells, opsins, and phototransduction cascades in diverse taxa, with a particular focus on cnidarians. In contrast to the common theme of deep homology, whereby similar traits develop mainly using homologous genes, comparisons of visual systems, especially in non-model organisms, are beginning to highlight a “deep diversity” of underlying components, illustrating how variation can underlie similar complex systems across taxa. Although using candidate genes from model organisms across diversity was a good starting point to understand the evolution of complex systems, unbiased genome-wide comparisons and subsequent functional validation will be necessary to uncover unique genes that comprise the complex systems of non-model groups to better understand biodiversity and its evolution. Full article
(This article belongs to the Special Issue Eye Development and Evolution: Cellular and Molecular Events)
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