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Michel Vervoort - One of the best experts on this subject based on the ideXlab platform.
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Zoological and molecular methods to study Annelida regeneration using Platynereis dumerilii in Methods in Molecular Biology. Editor: David Carroll. Springer
2021Co-Authors: Michel Vervoort, Eve GazaveAbstract:Regeneration, the ability to restore body parts after an injury or an amputation, is a widespread property in the animal kingdom. This chapter describes methods used to study this fascinating process in the annelid Platynereis dumerilii. During most of its life, this segmented worm is able to regenerate upon amputation the posterior part of its body, including its pygidium (terminal non-segmented body region bearing the anus) and a subterminal posterior growth zone which contains stem cells required for the formation of new segments. Detailed description of Platynereis worm culture and how to obtain large quantity of regenerating worms is provided. We also describe the staging system that we established and three important methods to study regeneration: whole-mount in situ hybridization to study gene expression, 5-ethynyl-2'-deoxyuridine (EdU) labeling to characterize cell proliferation, and use of pharmacological treatments to establish putative roles of defined signaling pathways and processes.
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posterior elongation in the annelid Platynereis dumerilii involves stem cells molecularly related to primordial germ cells
Developmental Biology, 2013Co-Authors: Eve Gazave, Adrien Demilly, Guillaume Balavoine, Julien Behague, Lucie Laplane, Aurelien Guillou, Laetitia Preau, Michel VervoortAbstract:Like most bilaterian animals, the annelid Platynereis dumerilii generates the majority of its body axis in an anterior to posterior temporal progression with new segments added sequentially. This process relies on a posterior subterminal proliferative body region, known as the “segment addition zone” (SAZ). We explored some of the molecular and cellular aspects of posterior elongation in Platynereis, in particular to test the hypothesis that the SAZ contains a specific set of stem cells dedicated to posterior elongation. We cloned and characterized the developmental expression patterns of orthologs of 17 genes known to be involved in the formation, behavior, or maintenance of stem cells in other metazoan models. These genes encode RNA-binding proteins (e.g., tudor, musashi, pumilio) or transcription factors (e.g., myc, id, runx) widely conserved in eumetazoans. Most of these genes are expressed both in the migrating primordial germ cells and in overlapping ring-like patterns in the SAZ, similar to some previously analyzed genes (piwi, vasa). The SAZ patterns are coincident with the expression of proliferation markers cyclin B and PCNA. EdU pulse and chase experiments suggest that new segments are produced through many rounds of divisions from small populations of teloblast-like posterior stem cells. The shared molecular signature between primordial germ cells and posterior stem cells in Platynereis thus corresponds to an ancestral “stemness” program.
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involvement of the wnt β catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature Communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Michel Vervoort, Eve GazaveAbstract:The Wnt/β-catenin pathway has important roles during neurogenesis in bilaterian animals. The authors show that this pathway regulates the transition from proliferating neural progenitors to differentiating neurons in the annelid Platynereis dumerilii, suggesting a conserved role in the last common bilaterian ancestor.
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Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature Communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Eve Gazave, Michel VervoortAbstract:The Wnt/β-catenin pathway has important roles during neurogenesis in bilaterian animals. The authors show that this pathway regulates the transition from proliferating neural progenitors to differentiating neurons in the annelid Platynereis dumerilii, suggesting a conserved role in the last common bilaterian ancestor.
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Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Eve Gazave, Michel VervoortAbstract:Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/β-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/β-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/β-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.
Gáspár Jékely - One of the best experts on this subject based on the ideXlab platform.
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neuronal cell types in the annelid Platynereis dumerilii
Current Opinion in Neurobiology, 2019Co-Authors: E Williams, Gáspár JékelyAbstract:The marine annelid Platynereis dumerilii is an invertebrate laboratory model for developmental biology and neuroscience. Its larval stages are small and transparent, enabling whole-body analyses of cell-type diversity and neuronal circuits. Here, we review the diversity of neuronal cell types in Platynereis. A variety of approaches have been used to identify cell types in Platynereis including whole-body gene expression atlases, single-cell RNA-seq and whole-body connectomics through serial EM reconstruction. The function of several cell types and neuronal circuits has also been analysed with experimental approaches. Platynereis has aspects of biology and cell types that are absent from the major invertebrate model organisms (C. elegans and Drosophila) including ciliary locomotion, noradrenergic neurons and ciliary photoreceptor cells.
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MOESM2 of Glass confers rhabdomeric photoreceptor identity in Drosophila, but not across all metazoans
2019Co-Authors: F. Bernardo-garcia, Gáspár Jékely, Maryam Syed, Simon SprecherAbstract:Additional file 2. Platynereis glass supplementary nucleotide sequences (both genomic and transcriptomic)
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MOESM6 of Glass confers rhabdomeric photoreceptor identity in Drosophila, but not across all metazoans
2019Co-Authors: F. Bernardo-garcia, Gáspár Jékely, Maryam Syed, Simon SprecherAbstract:Additional file 6. Annotated sequence of the glass-tomato plasmid that was used for Platynereis microinjections
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whole head recording of chemosensory activity in the marine annelid Platynereis dumerilii
bioRxiv, 2018Co-Authors: Thomas F Chartier, Joran Deschamps, Wiebke Duerichen, Gáspár Jékely, Detlev ArendtAbstract:Abstract Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensory studies. Here, we study the marine worm Platynereis dumerilii to provide the first comprehensive study of head chemosensory organ physiology in an annelid. By combining microfluidics and calcium imaging, we record neuronal activity in the entire head of early juveniles upon chemical stimulation. We find that Platynereis uses four types of organs to detect stimuli such as alcohols, esters, amino acids and sugars. Antennae, but not nuchal organs or palps as generally hypothesised in annelids, are the main chemosensory organs. We report chemically-evoked activity in possible downstream brain regions including the mushroom bodies, which are anatomically and molecularly similar to insect mushroom bodies. We conclude that chemosensation is a major sensory modality for marine annelids, and propose early Platynereis juveniles as a model to study annelid chemosensory systems.
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Chartier et al. 2018 - Supplementary video 3 - Oscillatory activity in the apical organ cells - speed x15.avi from Whole-head recording of chemosensory activity in the marine annelid Platynereis dumerilii
2018Co-Authors: Thomas F Chartier, Joran Deschamps, Gáspár Jékely, Wiebke Dürichen, Detlev ArendtAbstract:Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensory studies. Here, we study the marine worm Platynereis dumerilii to provide the first comprehensive study of head chemosensory organ physiology in an annelid. By combining microfluidics and calcium imaging, we record neuronal activity in the entire head of early juveniles upon chemical stimulation. We find that Platynereis uses four types of organs to detect stimuli such as alcohols, esters, amino acids and sugars. Antennae, but not nuchal organs or palps as generally hypothesized in annelids, are the main chemosensory organs. We report chemically evoked activity in possible downstream brain regions including the mushroom bodies (MBs), which are anatomically and molecularly similar to insect MBs. We conclude that chemosensation is a major sensory modality for marine annelids and propose early Platynereis juveniles as a model to study annelid chemosensory systems
Adrien Demilly - One of the best experts on this subject based on the ideXlab platform.
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posterior elongation in the annelid Platynereis dumerilii involves stem cells molecularly related to primordial germ cells
Developmental Biology, 2013Co-Authors: Eve Gazave, Adrien Demilly, Guillaume Balavoine, Julien Behague, Lucie Laplane, Aurelien Guillou, Laetitia Preau, Michel VervoortAbstract:Like most bilaterian animals, the annelid Platynereis dumerilii generates the majority of its body axis in an anterior to posterior temporal progression with new segments added sequentially. This process relies on a posterior subterminal proliferative body region, known as the “segment addition zone” (SAZ). We explored some of the molecular and cellular aspects of posterior elongation in Platynereis, in particular to test the hypothesis that the SAZ contains a specific set of stem cells dedicated to posterior elongation. We cloned and characterized the developmental expression patterns of orthologs of 17 genes known to be involved in the formation, behavior, or maintenance of stem cells in other metazoan models. These genes encode RNA-binding proteins (e.g., tudor, musashi, pumilio) or transcription factors (e.g., myc, id, runx) widely conserved in eumetazoans. Most of these genes are expressed both in the migrating primordial germ cells and in overlapping ring-like patterns in the SAZ, similar to some previously analyzed genes (piwi, vasa). The SAZ patterns are coincident with the expression of proliferation markers cyclin B and PCNA. EdU pulse and chase experiments suggest that new segments are produced through many rounds of divisions from small populations of teloblast-like posterior stem cells. The shared molecular signature between primordial germ cells and posterior stem cells in Platynereis thus corresponds to an ancestral “stemness” program.
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involvement of the wnt β catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature Communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Michel Vervoort, Eve GazaveAbstract:The Wnt/β-catenin pathway has important roles during neurogenesis in bilaterian animals. The authors show that this pathway regulates the transition from proliferating neural progenitors to differentiating neurons in the annelid Platynereis dumerilii, suggesting a conserved role in the last common bilaterian ancestor.
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Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature Communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Eve Gazave, Michel VervoortAbstract:The Wnt/β-catenin pathway has important roles during neurogenesis in bilaterian animals. The authors show that this pathway regulates the transition from proliferating neural progenitors to differentiating neurons in the annelid Platynereis dumerilii, suggesting a conserved role in the last common bilaterian ancestor.
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Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Eve Gazave, Michel VervoortAbstract:Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/β-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/β-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/β-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.
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involvement of the wnt β catenin pathway in neurectoderm architecture in Platynereis dumerilii
Nature Communications, 2013Co-Authors: Adrien Demilly, Patrick R H Steinmetz, Lauriane Marchand, Michel Vervoort, Eve GazaveAbstract:Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/β-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/β-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/β-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.
Kristin Tessmarraible - One of the best experts on this subject based on the ideXlab platform.
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a g o type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
BMC Biology, 2018Co-Authors: Thomas Ayers, Vinoth Babu Veedin Rajan, Kristin Tessmarraible, Martin Guhmann, Hisao TsukamotoAbstract:The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the Go-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii. We found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambdamax of approximately 490 nm. We show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex.
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talens mediate efficient and heritable mutation of endogenous genes in the marine annelid Platynereis dumerilii
Genetics, 2014Co-Authors: Stephanie C Bannister, Florian Raible, Olga Antonova, Alessandrea Polo, Natalia Hallay, Agne Valinciute, Claudia Lohs, Kristin TessmarraibleAbstract:Platynereis dumerilii is a marine polychaete and an established model system for studies of evolution and development. Platynereis is also a re-emerging model for studying the molecular basis of circalunar reproductive timing: a biological phenomenon observed in many marine species. While gene expression studies have provided new insight into patterns of gene regulation, a lack of reverse genetic tools has so far limited the depth of functional analyses in this species. To address this need, we established customized transcriptional activator-like effector nucleases (TALENs) as a tool to engineer targeted modifications in Platynereis genes. By adapting a workflow of TALEN construction protocols and mutation screening approaches for use in Platynereis, we engineered frameshift mutations in three endogenous Platynereis genes. We confirmed that such mutations are heritable, demonstrating that TALENs can be used to generate homozygous knockout lines in P. dumerilii. This is the first use of TALENs for generating genetic knockout mutations in an annelid model. These tools not only open the door for detailed in vivo functional analyses, but also can facilitate further technical development, such as targeted genome editing.
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stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution
Proceedings of the National Academy of Sciences of the United States of America, 2013Co-Authors: Benjamin Backfisch, Vinoth Babu Veedin Rajan, Kristin Tessmarraible, Claudia Lohs, Ruth M Fischer, Enrique Arboleda, Florian RaibleAbstract:Research in eye evolution has mostly focused on eyes residing in the head. In contrast, noncephalic light sensors are far less understood and rather regarded as evolutionary innovations. We established stable transgenesis in the annelid Platynereis, a reference species for evolutionary and developmental comparisons. EGFP controlled by cis-regulatory elements of r-opsin, a characteristic marker for rhabdomeric photoreceptors, faithfully recapitulates known r-opsin expression in the adult eyes, and marks a pair of pigment-associated frontolateral eyelets in the brain. Unexpectedly, transgenic animals revealed an additional series of photoreceptors in the ventral nerve cord as well as photoreceptors that are located in each pair of the segmental dorsal appendages (notopodia) and project into the ventral nerve cord. Consistent with a photosensory function of these noncephalic cells, decapitated animals display a clear photoavoidance response. Molecular analysis of the receptors suggests that they differentiate independent of pax6, a gene involved in early eye development of many metazoans, and that the ventral cells may share origins with the Hesse organs in the amphioxus neural tube. Finally, expression analysis of opn4×-2 and opn4m-2, two zebrafish orthologs of Platynereis r-opsin, reveals that these genes share expression in the neuromasts, known mechanoreceptors of the lateral line peripheral nervous system. Together, this establishes that noncephalic photoreceptors are more widespread than assumed, and may even reflect more ancient aspects of sensory systems. Our study marks significant advance for the understanding of photoreceptor cell (PRC) evolution and development and for Platynereis as a functional lophotrochozoan model system.
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vertebrate type intron rich genes in the marine annelid Platynereis dumerilii
Science, 2005Co-Authors: Florian Raible, Kristin Tessmarraible, Patrick Wincker, Claire Jubin, Guillaume Balavoine, Kazutoyo Osoegawa, Vladimir Benes, Pieter J. Jong, David E K Ferrier, Jean WeissenbachAbstract:Previous genome comparisons have suggested that one important trend in vertebrate evolution has been a sharp rise in intron abundance. By using genomic data and expressed sequence tags from the marine annelid Platynereis dumerilii, we provide direct evidence that about two-thirds of human introns predate the bilaterian radiation but were lost from insect and nematode genomes to a large extent. A comparison of coding exon sequences confirms the ancestral nature of Platynereis and human genes. Thus, the urbilaterian ancestor had complex, intron-rich genes that have been retained in Platynereis and human.
Vinoth Babu Veedin Rajan - One of the best experts on this subject based on the ideXlab platform.
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ciliary and rhabdomeric photoreceptor cell circuits form a spectral depth gauge in marine zooplankton
eLife, 2018Co-Authors: Vinoth Babu Veedin Rajan, Nadine Randel, Csaba Veraszto, Luis A Bezarescalderon, Martin Guhmann, Huiyong Jia, Cristina Pineirolopez, Reza ShahidiAbstract: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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a g o type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
BMC Biology, 2018Co-Authors: Thomas Ayers, Vinoth Babu Veedin Rajan, Kristin Tessmarraible, Martin Guhmann, Hisao TsukamotoAbstract:The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the Go-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii. We found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambdamax of approximately 490 nm. We show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex.
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A Go-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
BMC, 2018Co-Authors: Thomas Ayers, Vinoth Babu Veedin Rajan, Martin Guhmann, Hisao Tsukamoto, Kristin Tessmar-raibleAbstract:Abstract Background The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the Go-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii. Results We found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambdamax of approximately 490 nm. Conclusions We show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex
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Genetic and Genomic Tools for the Marine Annelid Platynereis dumerilii
Genetics, 2014Co-Authors: Juliane Zantke, Stephanie C Bannister, Vinoth Babu Veedin Rajan, Florian Raible, Kristin Tessmar-raibleAbstract:The bristle worm Platynereis dumerilii displays many interesting biological characteristics. These include its reproductive timing, which is synchronized to the moon phase, its regenerative capacity that is hormonally controlled, and a slow rate of evolution, which permits analyses of ancestral genes and cell types. As a marine annelid, Platynereis is also representative of the marine ecosystem, as well as one of the three large animal subphyla, the Lophotrochozoa. Here, we provide an overview of the molecular resources, functional techniques, and behavioral assays that have recently been established for the bristle worm. This combination of tools now places Platynereis in an excellent position to advance research at the frontiers of neurobiology, chronobiology, evo-devo, and marine biology.
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stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution
Proceedings of the National Academy of Sciences of the United States of America, 2013Co-Authors: Benjamin Backfisch, Vinoth Babu Veedin Rajan, Kristin Tessmarraible, Claudia Lohs, Ruth M Fischer, Enrique Arboleda, Florian RaibleAbstract:Research in eye evolution has mostly focused on eyes residing in the head. In contrast, noncephalic light sensors are far less understood and rather regarded as evolutionary innovations. We established stable transgenesis in the annelid Platynereis, a reference species for evolutionary and developmental comparisons. EGFP controlled by cis-regulatory elements of r-opsin, a characteristic marker for rhabdomeric photoreceptors, faithfully recapitulates known r-opsin expression in the adult eyes, and marks a pair of pigment-associated frontolateral eyelets in the brain. Unexpectedly, transgenic animals revealed an additional series of photoreceptors in the ventral nerve cord as well as photoreceptors that are located in each pair of the segmental dorsal appendages (notopodia) and project into the ventral nerve cord. Consistent with a photosensory function of these noncephalic cells, decapitated animals display a clear photoavoidance response. Molecular analysis of the receptors suggests that they differentiate independent of pax6, a gene involved in early eye development of many metazoans, and that the ventral cells may share origins with the Hesse organs in the amphioxus neural tube. Finally, expression analysis of opn4×-2 and opn4m-2, two zebrafish orthologs of Platynereis r-opsin, reveals that these genes share expression in the neuromasts, known mechanoreceptors of the lateral line peripheral nervous system. Together, this establishes that noncephalic photoreceptors are more widespread than assumed, and may even reflect more ancient aspects of sensory systems. Our study marks significant advance for the understanding of photoreceptor cell (PRC) evolution and development and for Platynereis as a functional lophotrochozoan model system.
